Comprehensive Physiology Wiley Online Library

Memory: Anatomical Organization of Candidate Brain Regions

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Relationship Between Association Cortices and Medial Temporal Lobe
2 Anatomy of Hippocampal Formation
2.1 Species Differences
2.2 Nomenclature
2.3 Subdivisions
2.4 Intrinsic Circuitry
2.5 Hippocampal Topography
2.6 Extrinsic Connections
2.7 Immunohistochemical Studies of Neuroactive Substances
3 Anatomy of Mamillary Complex
3.1 Intrinsic Organization
3.2 Afferents
3.3 Efferents
3.4 Connections of Associated Nuclei
4 Anatomy of Amygdaloid Complex
4.1 Nomenclature and Subdivisions
4.2 Intrinsic Circuitry
4.3 Extrinsic Connections
4.4 Neuroactive Substances
5 Comparison of Organization of Amygdaloid Complex and Hippocampal Formation
6 Anatomy of Mediodorsal Nucleus of Thalamus
6.1 Intrinsic Organization
6.2 Cortical Connections
6.3 Subcortical Connections
7 Neuropathology of Memory‐Related Structures in Alzheimer's Disease
7.1 Hippocampal Formation
7.2 Amygdaloid Complex
7.3 Mamillary Complex and Mediodorsal Thalamus
7.4 Loss of Neuroactive Substances in Alzheimer‐Affected Hippocampal Formation
8 Temporal Stem Hypothesis Revisited
9 Are There Additional Candidate Structures?
Figure 1. Figure 1.

Outlines of surface of macaque monkey brain show positions of major primary sensory cortices and of unimodal and polymodal association areas. Right: medial (top) and lateral (bottom) view of monkey brain. Primary visual cortex (VI), primary auditory cortex (AI), and primary somatosensory cortex (SI) are labeled, as is primary motor cortex (MI). Small numbers designate cortical fields as defined by Brodmann 69. AMG, amygdala; HIP, hippocampus, IPS, intraparietal sulcus; LF, lateral fissure; STS, superior temporal sulcus; TH and TF, fields of parahippocampal gyrus; TPO and PGa, polysensory fields on dorsal bank of superior temporal sulcus. Left: medial (top), lateral (middle), and ventral (bottom) surfaces of monkey brain. Approximate extents of primary (stippling) and secondary (vertical lines) unimodal association cortices are labeled. Positions of certain polysensory cortical regions (dotted shading) are also shown.

From Pandya and Seltzer 415
Figure 2. Figure 2.

Summary diagram showing progression of connections from primary sensory cortices to unimodal association cortices and finally to polymodal association areas. In each, dotted pattern shows projection origins and horizontal lines delimit termination regions. In somatosensory system, for example, primary somatosensory cortex (S) gives rise to projections to motor cortex (4) and to somatosensory association cortex (5). Area 5, in turn, gives rise to projections to premotor cortex (6) and to posterior parietal cortex (7). This latter region projects to polysensory zones in superior temporal sulcus (STS), cingulate gyrus (CG), and perirhinal cortex 35. A, primary auditory cortex; Am, amygdala; SM, supplementary motor cortex; STP, supratemporal plane; TG, temporal polar cortex.

Adapted from Jones and Powell 247
Figure 3. Figure 3.

Diagram illustrating progression of sensory information in visual system from primary visual cortex (OC) through successive association cortices (OB, OA, TEO, and TE) to amygdaloid complex. Unimodal visual input to amygdala arises from highest levels of hierarchy of cortical processing.

Adapted from Mishkin 367
Figure 4. Figure 4.

Four coronal sections through temporal lobe of macaque monkey brain (rostral to caudal) showing position of amygdaloid complex (A) and hippocampal formation (H) relative to other temporal lobe structures. Fibers that form portion of “temporal stem” (TS) are marked in B. Calibration marker, 5 mm. amts, Anterior middle temporal sulcus; f, fimbria; 51, piriform and periamygdaloid cortex; la, Id, Ig, insula cortex; ITG, inferior temporal gyrus; las, lateral sulcus; or, optic radiations; ots, occipitotemporal sulcus; pmts, posterior middle temporal sulcus; PU, putamen; PUL, pulvinar; rs, rhinal sulcus; STG, superior temporal gyrus; sts, superior temporal sulcus; TA, TE, TEO, TF, TG, TH, OA, OB, fields of temporal and occipital lobes according to Bailey and Bonin 29; 35/36, perirhinal cortex. For other abbreviations see Fig. 24 legend, p. 251.

Figure 5. Figure 5.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained human hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; EC, entorhinal cortex; f, fimbria; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum.

Figure 6. Figure 6.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained macaque monkey hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum; TE, visual association isocortex; TF/TH, polymodal association cortex of parahippocampal gyrus. For other abbreviations see Fig. 24 legend, p. 251.

Figure 7. Figure 7.

Surface maps showing demarcation, based on cytoarchitectonic criteria, of entorhinal cortex of humans (A) and macaque monkey (B) proposed by Rose 463. Similar map for monkey by Sgonina 508 is shown in C, and subdivisions of entorhinal cortex by Van Hoesen and Pandya 602 are illustrated in D. In each map, rostral is to left and mediodorsal is at top. Entorhinal cortex is differentiated along mediolateral and rostrocaudal gradients.

Figure 8. Figure 8.

Illustration of Golgi preparation from Lorente de Nó 326 shows principal cell types in dentate gyrus (fascia dentata) and CA1 hippocampal field (cornu ammonis). Main cell type in dentate gyrus is granule cell (cells 7–12), which has unipolar dendritic tree that extends into molecular layer. A second class of neurons, basket pyramidal cells (cell 13), gives rise to GABAergic basket plexus that terminates around the granule cell bodies. Principal cell in hippocampus is pyramidal cell (cells 1–5), which has apical dendritic plexus that extends into overlying strata radiatum and lacunosum‐moleculare, and basal dendritic plume that extends into subjacent stratum oriens. There are also several classes of inhibitory interneurons in hippocampus, some of which are located in pyramidal cell layer (cell 6) and in other strata as well.

From Lorente de Nó 326
Figure 9. Figure 9.

Illustration of Golgi‐stained neurons in mouse hippocampus from Lorente de Nó 326. Large cells of polymorphic region of dentate gyrus (cells 21 and 22, “mossy cells”) and pyramidal cells of the CA3 region (cells 8 and 10–19) have specialized spines (thorny excrescences) on their proximal dendrites, which are primary termination of mossy fibers from dentate gyrus. Interneuron of basket type is pictured as cell 9. Note that the pyramidal cells of CA2 region do not have large spines on their proximal dendrites and do not receive mossy fiber input. They are, however, much larger than adjoining pyramidal cells of CA1 region.

From Lorente de Nó 326
Figure 10. Figure 10.

Simplified circuit diagram demonstrating fundamental “trisynaptic” circuit of rat hippocampus. Fibers originating in entorhinal cortex (perforant path, pp) travel through subiculum and terminate on dendrites of granule cells in outer two‐thirds of molecular layer of dentate gyrus. Granule cells give rise to axons (mossy fibers, mf), which terminate on CA3 pyramidal cells. CA3 pyramidal cells project to CA1 region (Schaffer collaterals, sc). Because of “lamellar organization” of hippocampus, slices cut perpendicular to its long axis contain an intact chain of these connections.

Figure 11. Figure 11.

Line drawings of coronal section through monkey hippocampal formation on which major intrinsic and extrinsic efferent projections are plotted. A: various fields that comprise hippocampal formation are labeled and fundamental trisynaptic circuit is drawn [entorhinal cortex to dentate gyrus (1), dentate gyrus to hippocampal field CA3 (2), field CA3 to field CA1 (3)]. B: in addition to projecting to field CA3 (1), mossy fibers arising from dentate granule cells terminate on polymorphic cells of hilar region (2); these cells give rise to ipsilateral associational and commissural projections that terminate in molecular layer (3). CA3 pyramidal cells give rise to associational projections to other levels of field CA3 (5, 6) in addition to their projection to field CA1 (4). CA1 pyramidal cells project to subiculum (7), presubiculum (8), and entorhinal cortex (9). Cells in subiculum, presubiculum, and parasubiculum send a major projection to entorhinal cortex (10, 11, and 12, respectively). C: Projections to septal nuclei are diagramed. Field CA3 of hippocampus projects bilaterally to lateral septum (1) and field CA1 projects ipsilaterally (2). Subiculum also projects to lateral septum (3) and to nucleus accumbens (4). Entorhinal cortex projects to nucleus accumbens (5) and caudate nucleus and putamen (6). D: projections to diencephalon. Subiculum projects bilaterally to medial mamillary nucleus (1), whereas presubiculum projects primarily to lateral mamillary nucleus (2). Presubiculum also projects lightly to medial mamillary nucleus as does entorhinal cortex (3). Projection to anterior thalamus originates primarily in presubiculum and it terminates bilaterally (4). E: projections to amygdaloid complex. Both subiculum (1) and entorhinal cortex (2) project to parvicellular portion of basal nucleus; entorhinal cortex also projects to lateral nucleus (3). F: projections to neocortex. Although corticopetal projections of hippocampal formation are relatively unstudied, there is evidence for projections from both subicular complex and entorhinal cortex to cortical fields listed. AT, anterior thalamic nuclei; B, basal nucleus of amygdala; CA1, CA3, fields of hippocampus; DG, dentate gyrus; f, fornix; LM, lateral mamillary nucleus; LS, lateral septal nucleus; MM, medial mamillary nucleus; NA, nucleus accumbens; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. 24 legend, p. 251.

Figure 12. Figure 12.

Distribution of preterminal axons in entorhinal cortex arising from subfields of subicular complex. Projections from subiculum terminate in deep layers, whereas those from presubiculum end mainly in layer III and those from parasubiculum end in layer I.

From Köhler 273
Figure 13. Figure 13.

Summary diagram of commissural connections of monkey hippocampal formation. Top: extent of commissural fiber system is plotted (dotted lines) on lateral (left) and dorsal (right) views of brain. A: commissural projections of presubiculum and entorhinal cortex. Presubiculum (PrS) projects through hippocampal commissure (hc) to all levels of contralateral caudal entorhinal cortex (ECc). The ECc [but not rostral entorhinal cortex (ECr)] projects weakly to contralateral ECc and very lightly to posterior dentate gyrus (AD) and CA1 hippocampal field. B: rostral dentate gyrus and CA3 hippocampal field (H + AD) project to homotopic region of contralateral side. ab, Angular bundle; f, fimbria.

From Amaral et al. 13
Figure 14. Figure 14.

Ventromedial views of human (A) and macaque monkey (B) brains showing region of parahippocampal gyrus. cf, Calcarine fissure; cgs, cingulate sulcus; cos, collateral sulcus; ots, occipital temporal sulcus; rs, rhinal sulcus.

Courtesy of G. W. Van Hoesen
Figure 15. Figure 15.

Efferent projections of parahippocampal gyrus plotted on lateral (top) and medial (bottom) surfaces of macaque monkey brain. Numbers indicate cortical fields from nomenclature of Brodmann 69. Rsp, retrosplenial cortex.

Courtesy of G. W. Van Hoesen
Figure 16. Figure 16.

Photomicrographs of adjacent coronal sections through rostral hippocampal formation of monkey stained by Nissl method (A, bright field) or by immunohistochemical procedure for demonstration of somatostatin‐like immunoreactivity (B, dark‐field photomicrograph with immunoreactivity seen as light regions). Note particularly dense staining of molecular layer of dentate gyrus. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus (pl, polymorphic layer; ml, molecular layer); EC, entorhinal cortex; PaS, parasubiculum; PrS, presubiculum; rs, rhinal sulcus; S, subiculum. Small lettering in field CA1 indicates names of hippocampal laminae (a, alveus; o, stratum oriens; p, pyramidal cell layer; r, stratum radiatum; lm, stratum lacunosum‐moleculare). Calibration marker, 500 μm.

Figure 17. Figure 17.

Photomicrographs of coronal sections through macaque monkey mamillary complex arranged from rostral (A) to caudal (D). Each panel shows adjacent sections stained by Nissl method (top) or by reduced silver method for fibers (bottom). Calibration marker, 500 μm. f, Fornix; IC, intercalated nucleus; LMN, lateral mamillary nucleus; MMN, medial mamillary nucleus (MMNm pars medialis; MMNl, pars lateralis; MMNb, pars basalis); mp, mamillary peduncle; mtg, mamillotegmental tract; NG, nucleus gemini; PHN, posterior hypothalamic nucleus; pmt, principal mamillary tract; smc, supramamillary commissure; SUM, supramamillary area; TB, tuberomamillary nucleus. For other abbreviations see Fig. 24 legend, p. 251.

Figure 18. Figure 18.

Photomicrographs of adjacent sections through monkey mamillary complex stained as in Fig. 17. Main component of mamillary complex is medial nucleus (MMN), which can be divided into medial (M), lateral (L), and basal (MMNb) divisions. Other major component is lateral mamillary nucleus (LMN). Associated with mamillary complex are tuberomamillary nucleus (TB) and paramamillary nucleus (PM). Note in B the dense plexus of fibers that invest LMN. Principal mamillary tract (pmt) arises from dorsal surface of medial mamillary nucleus.

Figure 19. Figure 19.

Summary diagram of efferent connections of primate mamillary complex. Medial nucleus (MM) projects ipsilaterally via principal mamillary tract (pmt) and mamillothalamic tract (mth) to anteromedial (AM) and anteroventral (AV) subdivisions of anterior thalamus and also to ventral tegmental nucleus (VT) via mamillotegmental tract (mtg). Fibers from lateral mamillary nucleus (LM) use same pathways to project bilaterally to anterodorsal nucleus of thalamus (AD) and to dorsal tegmental nucleus (DT).

Figure 20. Figure 20.

Diagram of efferent connections of the 2 major subdivisions (areas 23 and 24) of cingulate cortex. Note that anterior cingulate (area 24) projects heavily to amygdaloid complex and to perirhinal and entorhinal cortices. Posterior cingulate cortex (area 23) has prominent projections to parahippocampal gyrus (TH‐TF) and presubiculum. AMG, amygdala; AS, arcuate sulcus; CC, corpus callosum; CF, calcarine fissure; CING S, cingulate sulcus; CS, central sulcus; IOS, inferior occipital sulcus; IPS, intraparietal sulcus; LB, basal nucleus of amygdala; LF, lateral fissure; LS, lunate sulcus; OS, orbital sulcus; OTS, occipital temporal sulcus; PAR HIPP, parahippocampal gyrus; POMS, parieto‐occipital medial sulcus; Presub, presubiculum; PS, principal sulcus; RS, rhinal sulcus; rspl c, retrosplenial cortex; STS, superior temporal sulcus.

From Pandya et al. 417
Figure 21. Figure 21.

Coronal section through the Nissl‐stained amygdaloid complex of macaque monkey. Major subdivisions of amygdala include lateral nucleus (L); basal nucleus, which has magnocellular (Bmg), parvicellular (Bpc), and paralaminar (Bpl) subdivisions; accessory basal nucleus, which has magnocellular (ABmg) and parvicellular (ABpc) divisions; central nucleus, which has medial (Cm) and lateral (Cl) divisions; medial nucleus (M); cortical area (CO); and periamygdaloid cortex (PAC). Entorhinal cortex (EC), bounded laterally by rhinal sulcus (rs), is also shown; the 6 principal laminae are numbered.

Figure 22. Figure 22.

Amygdaloid complex of shrew in its normal orientation (A) and after being rotated ventrolaterally (B). In B, positions of major nuclei closely resemble those of human amygdala. ABa, accessory basal nucleus, magnocellular division; ABb, accessory basal nucleus, parvicellular division; Ba, basal nucleus, magnocellular division; Bb, basal nucleus, parvicellular division; C, cortical area; CE, central nucleus; I, intercalated nucleus; L, lateral nucleus; M, medial nucleus; O, nucleus of lateral olfactory tract.

From Crosby and Humphrey 96
Figure 23. Figure 23.

Intrinsic connections of monkey amygdaloid complex. Local projections of lateral nucleus (A), basal nucleus (B), accessory basal nucleus (C), and central and medial nuclei and periamygdaloid cortex (D) are indicated. Arrows ending within origin nucleus indicate associational projections. Note tendency for laterally placed nuclei to project to central and medial nuclei. AB, accessory basal nucleus; Bmg, magnocellular division of basal nucleus; Bp, parvicellular division of basal nucleus; CI, lateral division of central nucleus; Cm, medial division of central nucleus. For other abbreviations see Fig. 24 legend, p. 251.

Figure 24. Figure 24.

Representative coronal sections through brain of macaque monkey, arranged from rostral (A) to caudal (L), showing distribution pattern of anterogradely labeled projections resulting from injection of tritiated amino acids into central nucleus of amygdala. Injection site is shown as blackened area in B and C. Labeled fibers are represented as dashed lines and terminal fields as dots. On left side of each section, triangles mark location of pigment‐containing, presumably monoaminergic neurons. ac, Anterior commissure; ACA, amygdaloclaustral area; AHA, amygdalohippocampal area; AM, anteromedial nucleus (thalamus); AN, arcuate nucleus (hypothalamus); AV, anteroventral nucleus (thalamus); BA, accessory basal nucleus (amygdala); BAm, accessory basal nucleus pars magnocellularis (amygdala); BAp, accessory basal nucleus pars parvocellularis (amygdala); bc, brachium conjunctivum; BL, basal nucleus (amygdala); BLm, basal nucleus pars magnocellularis (amygdala); BLp, basal nucleus pars parvicellularis (amygdala); BNM, basal nucleus of Meynert; BNST, bed nucleus of stria terminalis; bp, brachium pontis; C, central nucleus (amygdala); CBL, cerebellum; CD, caudate nucleus; Cde, nucleus centralis pars densocellularis (thalamus); CG, central gray; Cif, nucleus centralis inferior (thalamus); Cim, nucleus centralis intermedius (thalamus); CL, claustrum; Cl, nucleus centralis lateralis (thalamus); Clc, nucleus centralis pars laterocellularis (thalamus); CM, nucleus centralis medialis (thalamus); COa, anterior cortical nucleus (amygdala); COp, posterior cortical nucleus (amygdala); cp, cerebral peduncle; Cs, nucleus centralis superior (thalamus); CS, central superior raphe nucleus; DK, nucleus of Darkschewitsch; DM, dorsomedial nucleus (hypothalamus); DMN, dorsal motor nucleus of the vagus nerve; DR, dorsal raphe nucleus; EC, entorhinal cortex; EN, endopiriform nucleus; flm, medial longitudinal fasciculus; fm, fimbria; fx, fornix; GP, globus pallidus; GPe, globus pallidus (external); GPi, globus pallidus (internal); H, hippocampal formation; HB, habenular nuclei; HDB, horizontal limb of the nucleus of the diagonal band; IC, inferior colliculus; ic, internal capsule; IO, inferior olive; IP, interpeduncular nucleus; IS, interstitial nucleus; L, lateral nucleus (amygdala); LCd, nucleus locus coeruleus pars dorsalis; LCN, lateral cuneate nucleus; LCv, nucleus locus coeruleus pars ventralis; LD, laterodorsal nucleus (thalamus); If, lenticular fasciculus; LGN, lateral geniculate nucleus (thalamus); LH, lateral hypothalamus; LP, lateroposterior nucleus (thalamus); LR, lateral reticular nucleus; LT, lateral tuberal nucleus (hypothalamus); M, medial nucleus (amygdala); MD, mediodorsal nucleus (thalamus); MGN, medial geniculate nucleus (thalamus); Ml, lateral mamillary nucleus; ml, medial lemniscus; Mm, medial mamillary nucleus; NC, nucleus cuneiformis; NPC, nucleus of posterior commissure; NST, nucleus of solitary tract; NSTp, nucleus of solitary tract pars parvocellularis; oc, optic chiasm; ot, optic tract; P, putamen; PAC, periamygdaloid cortex; Pbl, lateral parabrachial nucleus; Pbm, medial parabrachial nucleus; pc, posterior commissure; PF, parafascicular nucleus; PH, nucleus prepositus hypoglossi; Pm, medial preoptic nucleus; PM, paramamillary nucleus; PN, pontine nuclei; PP, peripeduncular nucleus; PR, paramedian reticular nucleus; PRF, pontine reticular formation; PS, parasolitary nucleus; pt, pyramidal tract; PTA, pretectal area; PU, pulvinar nucleus; PUi, pulvinar nucleus pars inferior; PUl, pulvinar nucleus pars lateralis; PUm, pulvinar nucleus pars medialis; PV, periventricular nucleus (hypothalamus); Pv, ventral putamen; R, nucleus reticularis (thalamus); RE, nucleus reuniens (thalamus); RF, reticular formation; RM, nucleus raphe magnus; RN, red nucleus; RP, nucleus raphe pallidus; RTP, nucleus reticularis tegmenti pontis; SC, superior colliculus; SI, substantia innominata; sm, stria medullaris; SNc, substantia nigra pars compacta; SNr, substantia nigra pars reticulata; SO, superior olive; SON, supraoptic nucleus; ST, subthalamic nucleus; st, stria terminalis; tb, trapezoid body; TRF, tegmental reticular field; ts, solitary tract; V, ventricle; VA, nucleus ventralis anterior (thalamus); VDB, vertical limb of nucleus of diagonal band; Vl, inferior vestibular nucleus; VL, nucleus ventralis lateralis (thalamus); Vl, lateral vestibular nucleus; VM, ventromedial nucleus (hypothalamus); Vm, medial vestibular nucleus; VPL, nucleus ventralis posterolateralis (thalamus); VPM, nucleus ventralis posteromedialis (thalamus); Vs, superior vestibular nucleus; VTA, ventral tegmental area; ZI, zona incerta; 3, oculomotor nucleus; 4, trochlear nucleus; 6, abducens nucleus; 7, facial nucleus; 12, hypoglossal nucleus; M5, motor nucleus of trigeminal nerve; Me5, mesencephalic nucleus of trigeminal nerve; P5, principal nucleus of trigeminal nerve; S5, spinal nucleus of trigeminal nerve.

From Price and Amaral 439
Figure 25. Figure 25.

Representative coronal sections through forebrain of macaque monkey showing pattern of anterograde labeling after injection of amino acids into amygdaloid complex. Heaviest labeling is in nucleus accumbens (Ac), but there is also patchy labeling in caudate nucleus (Ca) and ventral portion of putamen (Pu). Labeling is particularly heavy in tail of caudate nucleus. Am, amygdala; Ca, caudate nucleus; CGL, lateral geniculate nucleus; Ch, cholinergic cell groups; GPv, globus pallidus, ventral division; OT, olfactory tubercle; ot, optic tract; PC, piriform cortex; Pu, putamen; Pul, pulvinar; R, red nucleus; S, septal nuclei. For other abbreviations see Fig. 24 legend, p. 251.

From Russchen et al. 473
Figure 26. Figure 26.

Illustration of amygdalohippocampal projections in monkey brain. Representative coronal section through amygdala is shown at left and coronal section through hippocampal formation is shown at right. ABmg, accessory basal nucleus, magnocellular division; ABpc, accessory basal nucleus, parvicellular division; Bmg, basal nucleus, magnocellular division; Bpc, basal nucleus, parvicellular division; CA1, CA3, hippocampal fields; CEl, central nucleus, lateral division; CEm, central nucleus, medial division; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. 24 legend, p. 251.

Figure 27. Figure 27.

A: illustrations of lateral, ventral, and medial surfaces of macaque monkey brain. Cortical fields indicated with nomenclature of Walker 629, Brodmann 69, and Bailey and Bonin 29. Insular cortex [dashed line surrounding lateral sulcus (Is)] is divided into agranular (la), dysgranular (Id), and granular (Ig) regions. B: shaded areas represent cortical regions that send direct projections to amygdala. C: shaded areas represent cortical regions that receive projections from amygdaloid complex. Question marks indicate that full extent of amygdaloid projections to these regions is not yet determined.

Figure 28. Figure 28.

Diagrams of lateral (left) and medial (right) surfaces of monkey, cat, and rat brains. Areas that project directly to amygdaloid complex are indicated by shading. Route by which sensory information attains these areas is also indicated (dashed arrows).

From Russchen 470
Figure 29. Figure 29.

Summary diagram showing topographic distribution of sensory projections to amygdaloid complex. Distribution of projections from sensory cortical areas (top panel) is indicated (with same stippling patterns) on 4 representative coronal sections through macaque monkey amygdala. a, Amygdaloid sulcus; AAA, anterior area of amygdala; AB, basal nucleus of amygdala; ABA, accessory basal nucleus of amygdala; AC, cortical nucleus of amygdala; ACA, claustral area of amygdala; ACe, central nucleus of amygdala; AL, lateral nucleus of amygdala; AM, medial nucleus of amygdala; C Ant, anterior commissure; Cd, caudate nucleus; CI, claustrum; Ea, entorhinal cortex, anterior part; En, endopiriform nucleus; erh, endorhinal sulcus; H, hippocampal formation; h, hippocampal sulcus; IA, insula cortex, anterior part; IB, insula cortex, posterior part; Pe, perirhinal cortex; Pi f, piriform cortex, frontal part; Pi t, piriform cortex; temporal part; Pr, prorhinal cortex; Put, putamen; rh, rhinal sulcus; SI‐B, substantia innominata—basal nucleus of Meynert; SI‐DB, substantia innominata—diagonal band; SOL, lateral olfactory stria; TA, superior temporal cortex; TE, inferior temporal cortex; TEO, inferior temporal cortex, posterior part; TG, temporal polar cortex; T Opt, optic tract; Tr, transition area; V Lat, lateral ventricle.

From Turner et al. 588
Figure 30. Figure 30.

Coronal section through macaque monkey thalamus. Mediodorsal nucleus is divided into magnocellular (or medial) (MDmc), parvicellular (or lateral) (MDpc), and multiform or paralaminar (MDmf) divisions.

From Olszewski 406
Figure 31. Figure 31.

Summary diagram of thalamic projections to monkey frontal cortex. Injections of retrograde tracers into regions (different shading patterns, top right) result in retrograde labeling of neurons in bands indicated in representative coronal sections of monkey thalamus at left. Panels (lower right) show same bands of labeling in horizontal sections through thalamus. A, anterior thalamus; CE, midline nuclei; CL, central lateral nucleus; CM‐PF, centromedian‐parafascicular complex; MGB, medial geniculate body; PCN, paracentral nucleus; PUL, pulvinar; VIM, ventral intermediate nucleus. For other abbreviations see Fig. 24 legend, p. 251.

From Kievit and Kuypers 262
Figure 32. Figure 32.

Diagrammatic summary of distribution of projections from various regions of frontal cortex to mediodorsal thalamus of macaque monkey. CM‐Pf, centromedian‐parafascicular complex; Cif, nucleus centralis, inferior division; MD, mediodorsal nucleus (mc, magnocellular division; pc, parvicellular division; mf, multiform or paralaminar division; de, densocellular division).

From Akert and Hartmann‐von Monakow 6
Figure 33. Figure 33.

Distribution of labeled cells after injection of retrograde tracer into magnocellular division of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al. 472
Figure 34. Figure 34.

Distribution of labeled cells after injection of retrograde tracer into parvicellular portion of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al. 472
Figure 35. Figure 35.

Distribution of neurofibrillary tangles (NFT) plotted onto coronal section of hippocampal formation from brain of patient with Alzheimer's disease. Each dot represents one neurofibrillary tangle. CA1, CA2–3, hippocampal fields; CA4, hilar region of dentate gyrus; NEO, neocortex; PRE, presubiculum; Pr2, prorhinal cortex; SUB, subiculum; 35, perirhinal cortex; 28, entorhinal cortex.

From Kemper 258
Figure 36. Figure 36.

Top: line drawings of coronal sections of human brain at levels through amygdaloid complex (left) and hippocampal formation (right); temporal stem (TEMP STEM) is labeled in each. Bottom: illustration showing dissection of left temporal lobe of human brain, which reveals fibers of temporal stem.

From Penfield 683


Figure 1.

Outlines of surface of macaque monkey brain show positions of major primary sensory cortices and of unimodal and polymodal association areas. Right: medial (top) and lateral (bottom) view of monkey brain. Primary visual cortex (VI), primary auditory cortex (AI), and primary somatosensory cortex (SI) are labeled, as is primary motor cortex (MI). Small numbers designate cortical fields as defined by Brodmann 69. AMG, amygdala; HIP, hippocampus, IPS, intraparietal sulcus; LF, lateral fissure; STS, superior temporal sulcus; TH and TF, fields of parahippocampal gyrus; TPO and PGa, polysensory fields on dorsal bank of superior temporal sulcus. Left: medial (top), lateral (middle), and ventral (bottom) surfaces of monkey brain. Approximate extents of primary (stippling) and secondary (vertical lines) unimodal association cortices are labeled. Positions of certain polysensory cortical regions (dotted shading) are also shown.

From Pandya and Seltzer 415


Figure 2.

Summary diagram showing progression of connections from primary sensory cortices to unimodal association cortices and finally to polymodal association areas. In each, dotted pattern shows projection origins and horizontal lines delimit termination regions. In somatosensory system, for example, primary somatosensory cortex (S) gives rise to projections to motor cortex (4) and to somatosensory association cortex (5). Area 5, in turn, gives rise to projections to premotor cortex (6) and to posterior parietal cortex (7). This latter region projects to polysensory zones in superior temporal sulcus (STS), cingulate gyrus (CG), and perirhinal cortex 35. A, primary auditory cortex; Am, amygdala; SM, supplementary motor cortex; STP, supratemporal plane; TG, temporal polar cortex.

Adapted from Jones and Powell 247


Figure 3.

Diagram illustrating progression of sensory information in visual system from primary visual cortex (OC) through successive association cortices (OB, OA, TEO, and TE) to amygdaloid complex. Unimodal visual input to amygdala arises from highest levels of hierarchy of cortical processing.

Adapted from Mishkin 367


Figure 4.

Four coronal sections through temporal lobe of macaque monkey brain (rostral to caudal) showing position of amygdaloid complex (A) and hippocampal formation (H) relative to other temporal lobe structures. Fibers that form portion of “temporal stem” (TS) are marked in B. Calibration marker, 5 mm. amts, Anterior middle temporal sulcus; f, fimbria; 51, piriform and periamygdaloid cortex; la, Id, Ig, insula cortex; ITG, inferior temporal gyrus; las, lateral sulcus; or, optic radiations; ots, occipitotemporal sulcus; pmts, posterior middle temporal sulcus; PU, putamen; PUL, pulvinar; rs, rhinal sulcus; STG, superior temporal gyrus; sts, superior temporal sulcus; TA, TE, TEO, TF, TG, TH, OA, OB, fields of temporal and occipital lobes according to Bailey and Bonin 29; 35/36, perirhinal cortex. For other abbreviations see Fig. 24 legend, p. 251.



Figure 5.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained human hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; EC, entorhinal cortex; f, fimbria; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum.



Figure 6.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained macaque monkey hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum; TE, visual association isocortex; TF/TH, polymodal association cortex of parahippocampal gyrus. For other abbreviations see Fig. 24 legend, p. 251.



Figure 7.

Surface maps showing demarcation, based on cytoarchitectonic criteria, of entorhinal cortex of humans (A) and macaque monkey (B) proposed by Rose 463. Similar map for monkey by Sgonina 508 is shown in C, and subdivisions of entorhinal cortex by Van Hoesen and Pandya 602 are illustrated in D. In each map, rostral is to left and mediodorsal is at top. Entorhinal cortex is differentiated along mediolateral and rostrocaudal gradients.



Figure 8.

Illustration of Golgi preparation from Lorente de Nó 326 shows principal cell types in dentate gyrus (fascia dentata) and CA1 hippocampal field (cornu ammonis). Main cell type in dentate gyrus is granule cell (cells 7–12), which has unipolar dendritic tree that extends into molecular layer. A second class of neurons, basket pyramidal cells (cell 13), gives rise to GABAergic basket plexus that terminates around the granule cell bodies. Principal cell in hippocampus is pyramidal cell (cells 1–5), which has apical dendritic plexus that extends into overlying strata radiatum and lacunosum‐moleculare, and basal dendritic plume that extends into subjacent stratum oriens. There are also several classes of inhibitory interneurons in hippocampus, some of which are located in pyramidal cell layer (cell 6) and in other strata as well.

From Lorente de Nó 326


Figure 9.

Illustration of Golgi‐stained neurons in mouse hippocampus from Lorente de Nó 326. Large cells of polymorphic region of dentate gyrus (cells 21 and 22, “mossy cells”) and pyramidal cells of the CA3 region (cells 8 and 10–19) have specialized spines (thorny excrescences) on their proximal dendrites, which are primary termination of mossy fibers from dentate gyrus. Interneuron of basket type is pictured as cell 9. Note that the pyramidal cells of CA2 region do not have large spines on their proximal dendrites and do not receive mossy fiber input. They are, however, much larger than adjoining pyramidal cells of CA1 region.

From Lorente de Nó 326


Figure 10.

Simplified circuit diagram demonstrating fundamental “trisynaptic” circuit of rat hippocampus. Fibers originating in entorhinal cortex (perforant path, pp) travel through subiculum and terminate on dendrites of granule cells in outer two‐thirds of molecular layer of dentate gyrus. Granule cells give rise to axons (mossy fibers, mf), which terminate on CA3 pyramidal cells. CA3 pyramidal cells project to CA1 region (Schaffer collaterals, sc). Because of “lamellar organization” of hippocampus, slices cut perpendicular to its long axis contain an intact chain of these connections.



Figure 11.

Line drawings of coronal section through monkey hippocampal formation on which major intrinsic and extrinsic efferent projections are plotted. A: various fields that comprise hippocampal formation are labeled and fundamental trisynaptic circuit is drawn [entorhinal cortex to dentate gyrus (1), dentate gyrus to hippocampal field CA3 (2), field CA3 to field CA1 (3)]. B: in addition to projecting to field CA3 (1), mossy fibers arising from dentate granule cells terminate on polymorphic cells of hilar region (2); these cells give rise to ipsilateral associational and commissural projections that terminate in molecular layer (3). CA3 pyramidal cells give rise to associational projections to other levels of field CA3 (5, 6) in addition to their projection to field CA1 (4). CA1 pyramidal cells project to subiculum (7), presubiculum (8), and entorhinal cortex (9). Cells in subiculum, presubiculum, and parasubiculum send a major projection to entorhinal cortex (10, 11, and 12, respectively). C: Projections to septal nuclei are diagramed. Field CA3 of hippocampus projects bilaterally to lateral septum (1) and field CA1 projects ipsilaterally (2). Subiculum also projects to lateral septum (3) and to nucleus accumbens (4). Entorhinal cortex projects to nucleus accumbens (5) and caudate nucleus and putamen (6). D: projections to diencephalon. Subiculum projects bilaterally to medial mamillary nucleus (1), whereas presubiculum projects primarily to lateral mamillary nucleus (2). Presubiculum also projects lightly to medial mamillary nucleus as does entorhinal cortex (3). Projection to anterior thalamus originates primarily in presubiculum and it terminates bilaterally (4). E: projections to amygdaloid complex. Both subiculum (1) and entorhinal cortex (2) project to parvicellular portion of basal nucleus; entorhinal cortex also projects to lateral nucleus (3). F: projections to neocortex. Although corticopetal projections of hippocampal formation are relatively unstudied, there is evidence for projections from both subicular complex and entorhinal cortex to cortical fields listed. AT, anterior thalamic nuclei; B, basal nucleus of amygdala; CA1, CA3, fields of hippocampus; DG, dentate gyrus; f, fornix; LM, lateral mamillary nucleus; LS, lateral septal nucleus; MM, medial mamillary nucleus; NA, nucleus accumbens; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. 24 legend, p. 251.



Figure 12.

Distribution of preterminal axons in entorhinal cortex arising from subfields of subicular complex. Projections from subiculum terminate in deep layers, whereas those from presubiculum end mainly in layer III and those from parasubiculum end in layer I.

From Köhler 273


Figure 13.

Summary diagram of commissural connections of monkey hippocampal formation. Top: extent of commissural fiber system is plotted (dotted lines) on lateral (left) and dorsal (right) views of brain. A: commissural projections of presubiculum and entorhinal cortex. Presubiculum (PrS) projects through hippocampal commissure (hc) to all levels of contralateral caudal entorhinal cortex (ECc). The ECc [but not rostral entorhinal cortex (ECr)] projects weakly to contralateral ECc and very lightly to posterior dentate gyrus (AD) and CA1 hippocampal field. B: rostral dentate gyrus and CA3 hippocampal field (H + AD) project to homotopic region of contralateral side. ab, Angular bundle; f, fimbria.

From Amaral et al. 13


Figure 14.

Ventromedial views of human (A) and macaque monkey (B) brains showing region of parahippocampal gyrus. cf, Calcarine fissure; cgs, cingulate sulcus; cos, collateral sulcus; ots, occipital temporal sulcus; rs, rhinal sulcus.

Courtesy of G. W. Van Hoesen


Figure 15.

Efferent projections of parahippocampal gyrus plotted on lateral (top) and medial (bottom) surfaces of macaque monkey brain. Numbers indicate cortical fields from nomenclature of Brodmann 69. Rsp, retrosplenial cortex.

Courtesy of G. W. Van Hoesen


Figure 16.

Photomicrographs of adjacent coronal sections through rostral hippocampal formation of monkey stained by Nissl method (A, bright field) or by immunohistochemical procedure for demonstration of somatostatin‐like immunoreactivity (B, dark‐field photomicrograph with immunoreactivity seen as light regions). Note particularly dense staining of molecular layer of dentate gyrus. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus (pl, polymorphic layer; ml, molecular layer); EC, entorhinal cortex; PaS, parasubiculum; PrS, presubiculum; rs, rhinal sulcus; S, subiculum. Small lettering in field CA1 indicates names of hippocampal laminae (a, alveus; o, stratum oriens; p, pyramidal cell layer; r, stratum radiatum; lm, stratum lacunosum‐moleculare). Calibration marker, 500 μm.



Figure 17.

Photomicrographs of coronal sections through macaque monkey mamillary complex arranged from rostral (A) to caudal (D). Each panel shows adjacent sections stained by Nissl method (top) or by reduced silver method for fibers (bottom). Calibration marker, 500 μm. f, Fornix; IC, intercalated nucleus; LMN, lateral mamillary nucleus; MMN, medial mamillary nucleus (MMNm pars medialis; MMNl, pars lateralis; MMNb, pars basalis); mp, mamillary peduncle; mtg, mamillotegmental tract; NG, nucleus gemini; PHN, posterior hypothalamic nucleus; pmt, principal mamillary tract; smc, supramamillary commissure; SUM, supramamillary area; TB, tuberomamillary nucleus. For other abbreviations see Fig. 24 legend, p. 251.



Figure 18.

Photomicrographs of adjacent sections through monkey mamillary complex stained as in Fig. 17. Main component of mamillary complex is medial nucleus (MMN), which can be divided into medial (M), lateral (L), and basal (MMNb) divisions. Other major component is lateral mamillary nucleus (LMN). Associated with mamillary complex are tuberomamillary nucleus (TB) and paramamillary nucleus (PM). Note in B the dense plexus of fibers that invest LMN. Principal mamillary tract (pmt) arises from dorsal surface of medial mamillary nucleus.



Figure 19.

Summary diagram of efferent connections of primate mamillary complex. Medial nucleus (MM) projects ipsilaterally via principal mamillary tract (pmt) and mamillothalamic tract (mth) to anteromedial (AM) and anteroventral (AV) subdivisions of anterior thalamus and also to ventral tegmental nucleus (VT) via mamillotegmental tract (mtg). Fibers from lateral mamillary nucleus (LM) use same pathways to project bilaterally to anterodorsal nucleus of thalamus (AD) and to dorsal tegmental nucleus (DT).



Figure 20.

Diagram of efferent connections of the 2 major subdivisions (areas 23 and 24) of cingulate cortex. Note that anterior cingulate (area 24) projects heavily to amygdaloid complex and to perirhinal and entorhinal cortices. Posterior cingulate cortex (area 23) has prominent projections to parahippocampal gyrus (TH‐TF) and presubiculum. AMG, amygdala; AS, arcuate sulcus; CC, corpus callosum; CF, calcarine fissure; CING S, cingulate sulcus; CS, central sulcus; IOS, inferior occipital sulcus; IPS, intraparietal sulcus; LB, basal nucleus of amygdala; LF, lateral fissure; LS, lunate sulcus; OS, orbital sulcus; OTS, occipital temporal sulcus; PAR HIPP, parahippocampal gyrus; POMS, parieto‐occipital medial sulcus; Presub, presubiculum; PS, principal sulcus; RS, rhinal sulcus; rspl c, retrosplenial cortex; STS, superior temporal sulcus.

From Pandya et al. 417


Figure 21.

Coronal section through the Nissl‐stained amygdaloid complex of macaque monkey. Major subdivisions of amygdala include lateral nucleus (L); basal nucleus, which has magnocellular (Bmg), parvicellular (Bpc), and paralaminar (Bpl) subdivisions; accessory basal nucleus, which has magnocellular (ABmg) and parvicellular (ABpc) divisions; central nucleus, which has medial (Cm) and lateral (Cl) divisions; medial nucleus (M); cortical area (CO); and periamygdaloid cortex (PAC). Entorhinal cortex (EC), bounded laterally by rhinal sulcus (rs), is also shown; the 6 principal laminae are numbered.



Figure 22.

Amygdaloid complex of shrew in its normal orientation (A) and after being rotated ventrolaterally (B). In B, positions of major nuclei closely resemble those of human amygdala. ABa, accessory basal nucleus, magnocellular division; ABb, accessory basal nucleus, parvicellular division; Ba, basal nucleus, magnocellular division; Bb, basal nucleus, parvicellular division; C, cortical area; CE, central nucleus; I, intercalated nucleus; L, lateral nucleus; M, medial nucleus; O, nucleus of lateral olfactory tract.

From Crosby and Humphrey 96


Figure 23.

Intrinsic connections of monkey amygdaloid complex. Local projections of lateral nucleus (A), basal nucleus (B), accessory basal nucleus (C), and central and medial nuclei and periamygdaloid cortex (D) are indicated. Arrows ending within origin nucleus indicate associational projections. Note tendency for laterally placed nuclei to project to central and medial nuclei. AB, accessory basal nucleus; Bmg, magnocellular division of basal nucleus; Bp, parvicellular division of basal nucleus; CI, lateral division of central nucleus; Cm, medial division of central nucleus. For other abbreviations see Fig. 24 legend, p. 251.



Figure 24.

Representative coronal sections through brain of macaque monkey, arranged from rostral (A) to caudal (L), showing distribution pattern of anterogradely labeled projections resulting from injection of tritiated amino acids into central nucleus of amygdala. Injection site is shown as blackened area in B and C. Labeled fibers are represented as dashed lines and terminal fields as dots. On left side of each section, triangles mark location of pigment‐containing, presumably monoaminergic neurons. ac, Anterior commissure; ACA, amygdaloclaustral area; AHA, amygdalohippocampal area; AM, anteromedial nucleus (thalamus); AN, arcuate nucleus (hypothalamus); AV, anteroventral nucleus (thalamus); BA, accessory basal nucleus (amygdala); BAm, accessory basal nucleus pars magnocellularis (amygdala); BAp, accessory basal nucleus pars parvocellularis (amygdala); bc, brachium conjunctivum; BL, basal nucleus (amygdala); BLm, basal nucleus pars magnocellularis (amygdala); BLp, basal nucleus pars parvicellularis (amygdala); BNM, basal nucleus of Meynert; BNST, bed nucleus of stria terminalis; bp, brachium pontis; C, central nucleus (amygdala); CBL, cerebellum; CD, caudate nucleus; Cde, nucleus centralis pars densocellularis (thalamus); CG, central gray; Cif, nucleus centralis inferior (thalamus); Cim, nucleus centralis intermedius (thalamus); CL, claustrum; Cl, nucleus centralis lateralis (thalamus); Clc, nucleus centralis pars laterocellularis (thalamus); CM, nucleus centralis medialis (thalamus); COa, anterior cortical nucleus (amygdala); COp, posterior cortical nucleus (amygdala); cp, cerebral peduncle; Cs, nucleus centralis superior (thalamus); CS, central superior raphe nucleus; DK, nucleus of Darkschewitsch; DM, dorsomedial nucleus (hypothalamus); DMN, dorsal motor nucleus of the vagus nerve; DR, dorsal raphe nucleus; EC, entorhinal cortex; EN, endopiriform nucleus; flm, medial longitudinal fasciculus; fm, fimbria; fx, fornix; GP, globus pallidus; GPe, globus pallidus (external); GPi, globus pallidus (internal); H, hippocampal formation; HB, habenular nuclei; HDB, horizontal limb of the nucleus of the diagonal band; IC, inferior colliculus; ic, internal capsule; IO, inferior olive; IP, interpeduncular nucleus; IS, interstitial nucleus; L, lateral nucleus (amygdala); LCd, nucleus locus coeruleus pars dorsalis; LCN, lateral cuneate nucleus; LCv, nucleus locus coeruleus pars ventralis; LD, laterodorsal nucleus (thalamus); If, lenticular fasciculus; LGN, lateral geniculate nucleus (thalamus); LH, lateral hypothalamus; LP, lateroposterior nucleus (thalamus); LR, lateral reticular nucleus; LT, lateral tuberal nucleus (hypothalamus); M, medial nucleus (amygdala); MD, mediodorsal nucleus (thalamus); MGN, medial geniculate nucleus (thalamus); Ml, lateral mamillary nucleus; ml, medial lemniscus; Mm, medial mamillary nucleus; NC, nucleus cuneiformis; NPC, nucleus of posterior commissure; NST, nucleus of solitary tract; NSTp, nucleus of solitary tract pars parvocellularis; oc, optic chiasm; ot, optic tract; P, putamen; PAC, periamygdaloid cortex; Pbl, lateral parabrachial nucleus; Pbm, medial parabrachial nucleus; pc, posterior commissure; PF, parafascicular nucleus; PH, nucleus prepositus hypoglossi; Pm, medial preoptic nucleus; PM, paramamillary nucleus; PN, pontine nuclei; PP, peripeduncular nucleus; PR, paramedian reticular nucleus; PRF, pontine reticular formation; PS, parasolitary nucleus; pt, pyramidal tract; PTA, pretectal area; PU, pulvinar nucleus; PUi, pulvinar nucleus pars inferior; PUl, pulvinar nucleus pars lateralis; PUm, pulvinar nucleus pars medialis; PV, periventricular nucleus (hypothalamus); Pv, ventral putamen; R, nucleus reticularis (thalamus); RE, nucleus reuniens (thalamus); RF, reticular formation; RM, nucleus raphe magnus; RN, red nucleus; RP, nucleus raphe pallidus; RTP, nucleus reticularis tegmenti pontis; SC, superior colliculus; SI, substantia innominata; sm, stria medullaris; SNc, substantia nigra pars compacta; SNr, substantia nigra pars reticulata; SO, superior olive; SON, supraoptic nucleus; ST, subthalamic nucleus; st, stria terminalis; tb, trapezoid body; TRF, tegmental reticular field; ts, solitary tract; V, ventricle; VA, nucleus ventralis anterior (thalamus); VDB, vertical limb of nucleus of diagonal band; Vl, inferior vestibular nucleus; VL, nucleus ventralis lateralis (thalamus); Vl, lateral vestibular nucleus; VM, ventromedial nucleus (hypothalamus); Vm, medial vestibular nucleus; VPL, nucleus ventralis posterolateralis (thalamus); VPM, nucleus ventralis posteromedialis (thalamus); Vs, superior vestibular nucleus; VTA, ventral tegmental area; ZI, zona incerta; 3, oculomotor nucleus; 4, trochlear nucleus; 6, abducens nucleus; 7, facial nucleus; 12, hypoglossal nucleus; M5, motor nucleus of trigeminal nerve; Me5, mesencephalic nucleus of trigeminal nerve; P5, principal nucleus of trigeminal nerve; S5, spinal nucleus of trigeminal nerve.

From Price and Amaral 439


Figure 25.

Representative coronal sections through forebrain of macaque monkey showing pattern of anterograde labeling after injection of amino acids into amygdaloid complex. Heaviest labeling is in nucleus accumbens (Ac), but there is also patchy labeling in caudate nucleus (Ca) and ventral portion of putamen (Pu). Labeling is particularly heavy in tail of caudate nucleus. Am, amygdala; Ca, caudate nucleus; CGL, lateral geniculate nucleus; Ch, cholinergic cell groups; GPv, globus pallidus, ventral division; OT, olfactory tubercle; ot, optic tract; PC, piriform cortex; Pu, putamen; Pul, pulvinar; R, red nucleus; S, septal nuclei. For other abbreviations see Fig. 24 legend, p. 251.

From Russchen et al. 473


Figure 26.

Illustration of amygdalohippocampal projections in monkey brain. Representative coronal section through amygdala is shown at left and coronal section through hippocampal formation is shown at right. ABmg, accessory basal nucleus, magnocellular division; ABpc, accessory basal nucleus, parvicellular division; Bmg, basal nucleus, magnocellular division; Bpc, basal nucleus, parvicellular division; CA1, CA3, hippocampal fields; CEl, central nucleus, lateral division; CEm, central nucleus, medial division; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. 24 legend, p. 251.



Figure 27.

A: illustrations of lateral, ventral, and medial surfaces of macaque monkey brain. Cortical fields indicated with nomenclature of Walker 629, Brodmann 69, and Bailey and Bonin 29. Insular cortex [dashed line surrounding lateral sulcus (Is)] is divided into agranular (la), dysgranular (Id), and granular (Ig) regions. B: shaded areas represent cortical regions that send direct projections to amygdala. C: shaded areas represent cortical regions that receive projections from amygdaloid complex. Question marks indicate that full extent of amygdaloid projections to these regions is not yet determined.



Figure 28.

Diagrams of lateral (left) and medial (right) surfaces of monkey, cat, and rat brains. Areas that project directly to amygdaloid complex are indicated by shading. Route by which sensory information attains these areas is also indicated (dashed arrows).

From Russchen 470


Figure 29.

Summary diagram showing topographic distribution of sensory projections to amygdaloid complex. Distribution of projections from sensory cortical areas (top panel) is indicated (with same stippling patterns) on 4 representative coronal sections through macaque monkey amygdala. a, Amygdaloid sulcus; AAA, anterior area of amygdala; AB, basal nucleus of amygdala; ABA, accessory basal nucleus of amygdala; AC, cortical nucleus of amygdala; ACA, claustral area of amygdala; ACe, central nucleus of amygdala; AL, lateral nucleus of amygdala; AM, medial nucleus of amygdala; C Ant, anterior commissure; Cd, caudate nucleus; CI, claustrum; Ea, entorhinal cortex, anterior part; En, endopiriform nucleus; erh, endorhinal sulcus; H, hippocampal formation; h, hippocampal sulcus; IA, insula cortex, anterior part; IB, insula cortex, posterior part; Pe, perirhinal cortex; Pi f, piriform cortex, frontal part; Pi t, piriform cortex; temporal part; Pr, prorhinal cortex; Put, putamen; rh, rhinal sulcus; SI‐B, substantia innominata—basal nucleus of Meynert; SI‐DB, substantia innominata—diagonal band; SOL, lateral olfactory stria; TA, superior temporal cortex; TE, inferior temporal cortex; TEO, inferior temporal cortex, posterior part; TG, temporal polar cortex; T Opt, optic tract; Tr, transition area; V Lat, lateral ventricle.

From Turner et al. 588


Figure 30.

Coronal section through macaque monkey thalamus. Mediodorsal nucleus is divided into magnocellular (or medial) (MDmc), parvicellular (or lateral) (MDpc), and multiform or paralaminar (MDmf) divisions.

From Olszewski 406


Figure 31.

Summary diagram of thalamic projections to monkey frontal cortex. Injections of retrograde tracers into regions (different shading patterns, top right) result in retrograde labeling of neurons in bands indicated in representative coronal sections of monkey thalamus at left. Panels (lower right) show same bands of labeling in horizontal sections through thalamus. A, anterior thalamus; CE, midline nuclei; CL, central lateral nucleus; CM‐PF, centromedian‐parafascicular complex; MGB, medial geniculate body; PCN, paracentral nucleus; PUL, pulvinar; VIM, ventral intermediate nucleus. For other abbreviations see Fig. 24 legend, p. 251.

From Kievit and Kuypers 262


Figure 32.

Diagrammatic summary of distribution of projections from various regions of frontal cortex to mediodorsal thalamus of macaque monkey. CM‐Pf, centromedian‐parafascicular complex; Cif, nucleus centralis, inferior division; MD, mediodorsal nucleus (mc, magnocellular division; pc, parvicellular division; mf, multiform or paralaminar division; de, densocellular division).

From Akert and Hartmann‐von Monakow 6


Figure 33.

Distribution of labeled cells after injection of retrograde tracer into magnocellular division of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al. 472


Figure 34.

Distribution of labeled cells after injection of retrograde tracer into parvicellular portion of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al. 472


Figure 35.

Distribution of neurofibrillary tangles (NFT) plotted onto coronal section of hippocampal formation from brain of patient with Alzheimer's disease. Each dot represents one neurofibrillary tangle. CA1, CA2–3, hippocampal fields; CA4, hilar region of dentate gyrus; NEO, neocortex; PRE, presubiculum; Pr2, prorhinal cortex; SUB, subiculum; 35, perirhinal cortex; 28, entorhinal cortex.

From Kemper 258


Figure 36.

Top: line drawings of coronal sections of human brain at levels through amygdaloid complex (left) and hippocampal formation (right); temporal stem (TEMP STEM) is labeled in each. Bottom: illustration showing dissection of left temporal lobe of human brain, which reveals fibers of temporal stem.

From Penfield 683
References
 1. Aggleton, J. P. A description of intra‐amygdaloid connections in old world monkeys. Exp. Brain Res. 57: 390–399, 1985.
 2. Aggleton, J. P., M. J. Burton, and R. E. Passingham. Cortical and subcortical afferents to the amygdala of the rhesus monkey. Brain Res. 190: 347–368, 1980.
 3. Aggleton, J. P., and M. Mishkin. Memory impairments following restricted medial thalamic lesions in monkeys. Exp. Brain Res. 52: 199–209, 1983.
 4. Aggleton, J. P., and M. Mishkin. Visual recognition impairment following medial thalamic lesions in monkeys. Neuropsychologia 21: 189–197, 1983.
 5. Aggleton, J. P., and M. Mishkin. Projections of the amygdala to the thalamus in the cynomolgus monkey. J. Comp. Neurol. 222: 56–58, 1984.
 6. Akert, K., and K. Hartmann‐von Monakow. Relationships of precentral, premotor, and prefrontal cortex to the mediodorsal and intralaminar nuclei of the monkey thalamus. Acta Neurobiol. Exp. 40: 7–25, 1980.
 7. Alonso, A., and C. Köhler. Evidence for separate projections of hippocampal pyramidal and non‐pyramidal neurons to different parts of the septum in the rat brain. Neurosci. Lett. 31: 209–214, 1982.
 8. Alonso, A., and C. Köhler. A study of the reciprocal connections between the septum and the entorhinal area using anterograde and retrograde axonal transport methods in thé rat brain. J. Comp. Neurol. 225: 327–343, 1984.
 9. Amaral, D. G. A Golgi study of the cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182: 851–914, 1978.
 10. Amaral, D. G. Amygdalohippocampal and amygdalocortical projections in the primate brain. In: Excitatory Amino Acids and Epilepsy, edited by Y. Ben‐Ari and R. Schwarcz. New York: Plenum, 1986, p. 3–17.
 11. Amaral, D. G., and M. J. Campbell. Transmitter systems in the primate dentate gyrus. Hum. Neurobiol. 5: 169–180, 1986.
 12. Amaral, D. G., and W. M. Cowan. Subcortical afferents to the hippocampal formation in the monkey. J. Comp. Neurol. 189: 573–591, 1980.
 13. Amaral, D. G., R. Insausti, and W. M. Cowan. Evidence for a direct projection from the superior temporal gyrus to the entorhinal cortex in the monkey. Brain Res. 275: 263–277, 1983.
 14. Amaral, D. G., R. Insausti, and W. M. Cowan. The commissural connections of the monkey hippocampal formation. J. Comp. Neurol. 224: 307–336, 1984.
 15. Amaral, D. G., R. Insausti, and W. M. Cowan. The monkey entorhinal cortex. I. Cytoarchitectonic organization. J. Comp. Neurol. In press.
 16. Amaral, D. G., and J. Kurz. An analysis of the origins of the cholinergic and non‐cholinergic septal projections to the hippocampal formation of the rat. J. Comp. Neurol. 240: 37–59, 1985.
 17. Amaral, D. G., and J. L. Price. Amygdalo‐cortical projections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230: 465–496, 1984.
 18. Amaral, D. G., R. B. Veazey, and W. M. Cowan. Some observations on hypothalamo‐amygdaloid connections in the monkey. Brain Res. 252: 13–27, 1982.
 19. Andersen, P. Operational principles of hippocampal neurons. In: Neurobiology of the Hippocampus, edited by W. Seifert. New York: Academic, 1983, p. 81–86.
 20. Andersen, P., T. V. P. Bliss, and K. K. Skrede. Lamellar organization of hippocampal excitatory pathways. Exp. Brain Res. 13: 222–238, 1971.
 21. Andersen, P., J. C. Eccles, and Y. Loyning. Recurrent inhibition in the hippocampus with identification of the inhibitory cell and synapses. Nature Lond. 198: 540–542, 1963.
 22. Andersen, P., B. Holmquist, and P. E. Voorhoeve. Entorhinal activation of dentate granule cells. Acta Physiol. Scand. 66: 448–460, 1966.
 23. Arai, H., K. Kosaka, and R. Iizuka. Changes of biogenic amines and their metabolites in postmortem brain from patients with Alzheimer‐type dementia. J. Neurochem. 43: 388–393, 1984.
 24. Arendt, T., V. Bigl, A. Arendt, and A. Tennstedt. Loss of neurons in the nucleus basalis of Meynert in Alzheimer's disease, paralysis agitans and Korsakoff's disease. Acta Neuropathol. 61: 101–108, 1983.
 25. Arikuni, T., M. Sakai, and K. Kubota. Columnar aggregation of prefrontal and anterior cingulate cortical cells projecting to the thalamic mediodorsal nucleus in the monkey. J. Comp. Neurol. 220: 116–125, 1983.
 26. Atweh, S. F., and M. H. Kuhar. Autoradiographic localization of opiate receptors in rat brain. III. The telencephalon. Brain Res. 134: 393–405, 1977.
 27. Avendano, C., J. L. Price, and D. G. Amaral. Evidence for an amygdaloid projection to premotor cortex but not to motor cortex in the monkey. Brain Res. 264: 111–117, 1983.
 28. Azmitia, E. C., and M. Segal. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. Comp. Neurol. 179: 641–668, 1978.
 29. Bailey, P., and G. von Bonin. The Isocortex of Man. Urbana: Univ. of Illinois Press, 1951.
 30. Baisden, R. H., M. L. Woodruff, and D. B. Hoover. Cholinergic and non‐cholinergic septo‐hippocampal projections: a double‐label horseradish peroxidase‐acetylcholinesterase study in the rabbit. Brain Res. 290: 146–151, 1984.
 31. Bakst, I., and D. G. Amaral. The distribution of acetylcholinesterase in the hippocampal formation of the monkey. J. Comp. Neurol. 225: 344–371, 1984.
 32. Bakst, I., C. Avendano, J. H. Morrison, and D. G. Amaral. An experimental analysis of the origins of the somatostatin immunoreactive fibers in the dentate gyrus of the rat. J. Neurosci. 6: 1452–1462, 1986.
 33. Bakst, I., J. H. Morrison, and D. G. Amaral. The distribution of somatostatin‐like immunoreactivity in the monkey hippocampal formation. J. Comp. Neurol. 236: 423–442, 1985.
 34. Baleydier, C., and F. Mauguiere. The duality of the cingulate gyrus in the monkey. Neuoranatomical study and functional hypothesis. Brain 103: 525–554, 1980.
 35. Ball, M. J. Neuronal loss, neurofibrillary tangles and granu‐lovacuolar degeneration in the hippocampus with ageing and dementia. Acta Neuropathol. 37: 111–118, 1977.
 36. Ball, M. J. Topographic distribution of neurofibrillary tangles and granulovacuolar degeneration in hippocampal cortex of aging and demented patients. A quantitative study. Acta Neuropathol. 42: 73–80, 1978.
 37. Ball, M. J. Granulovacuolar degeneration. In: Alzheimer's Disease, edited by B. Reisberg. New York: Free Press, 1983, p. 62–68.
 38. Ball, M. J., M. Fisman, V. Hachinski, W. Blume, A. Fox, V. A. Kral, A. J. Kirshen, H. Fox, and H. Merskey. A new definition of Alzheimer's disease: a hippocampal dementia. Lancet 1: 14–16, 1985.
 39. Ball, M. J., H. Merskey, M. Fisman, I. M. Fyfe, H. Fox, R. D. T. Cape, S. B. Waller, and E. D. London. Hippocampal morphometry in Alzheimer dementia: implications of neurochemical hypotheses. In: Banbury Report. Biological Aspects of Alzheimer's Disease, edited by R. Katzman. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1983, vol. 15, p. 45–64.
 40. Barbizet, J. Defect of memorizing of hippocampal‐mamillary origin: a review. J. Neurol. Neurosurg. Psychiatry 26: 127–135, 1963.
 41. Barden, N., Y. Merand, D. Rouleau, S. Moore, G. J. Dockray, and A. Dupont. Regional distributions of somatostatin and cholecystokinin‐like immunoreactivities in rat and bovine brain. Peptides Fayetteville 2: 299–302, 1981.
 42. Bechterew, W. W. Demonstration eines Gehirns mit Zerstörung der vorderen und inneren theile der Hirnrinde beider Schlafenlappen. Neurologisches Centralblatt 19: 990–991, 1900.
 43. Beckstead, R. M. Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell‐labeling with horseradish peroxidase. Brain Res. 152: 249–264, 1978.
 44. Beckstead, R. M. An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal‐projection (prefrontal) cortex in the rat. J. Comp. Neurol. 184: 43–62, 1979.
 45. Beckstead, R. M. The thalamostriatal projection in the cat. J. Comp. Neurol. 223: 313–346, 1984.
 46. Beckstead, R. M., V. B. Domesick, and W. J. Nauta. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175: 191–217, 1979.
 47. Beckstead, R. M., J. R. Morse, and R. Norgren. The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei. J. Comp. Neurol. 190: 259–282, 1980.
 48. Ben‐Ari, Y. Transmitters and modulators in the amygdaloid complex: a review. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 163–174.
 49. Ben‐Ari, Y., I. Kanazawa, and R. E. Zigmond. Regional distribution of glutamate decarboxylase and gaba within the amygdaloid complex and stria terminalis system of the rat. J. Neurochem. 26: 1279–1283, 1976.
 50. Ben‐Ari, Y., G. Le Gal La Salle, G. Barbin, J. C. Schwartz, and M. Garbarg. Histamine synthesizing afferents within the amygdaloid complex and bed nucleus of the stria terminalis of the rat. Brain Res. 138: 285–294, 1977.
 51. Ben‐Ari, Y., R. E. Zigmond, and K. E. Moore. Regional distribution of tyrosine hydroxylase, norepinephrine and dopamine within the amygdaloid complex of the rat. Brain Res. 87: 96–101, 1975.
 52. Ben‐Ari, Y., R. E. Zigmond, C. C. Shute, and P. R. Lewis. Regional distribution of choline acetyltransferase and acetylcholinesterase within the amygdaloid complex and stria terminalis system. Brain Res. 120: 435–444, 1977.
 53. Benevento, I. A., J. Fallon, B. J. Davisk, and M. Rezak. Auditory‐visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey. Exp. Neurol. 57: 849–872, 1977.
 54. Benjamin, R. M., and J. C. Jackson. Unit discharges in the mediodorsal nucleus of the squirrel monkey evoked by electrical stimulation of the olfactory bulb. Brain Res. 75: 181–191, 1974.
 55. Benjamin, R. M., J. C. Jackson, G. T. Golden, and C. H. K. West. Sources of olfactory inputs to opossum mediodorsal nucleus identified by horseradish peroxidase and autoradiographic methods. J. Comp. Neurol. 207: 358–368, 1982.
 56. Bentivoglio, M., G. Macchi, P. Rossini, and E. Tempesta. Brain stem neurons projecting to neocortex: a HRP study in the cat. Exp. Brain Res. 31: 489–498, 1978.
 57. Besson, J., M. Dussaillant, J. C. Marie, W. Rostene, and G. Rosselin. In vitro autoradiographic localization of vasoactive intestinal peptide (VIP) binding sites in the rat central nervous system. Peptides Fayetteville 5: 339–340, 1984.
 58. Biegon, A., T. C. Rainbow, J. J. Mann, and B. S. McEwen. Neurotransmitter receptor sites in human hippocampus: a quantitative autoradiographic study. Brain Res. 247: 379–382, 1982.
 59. Blackstad, T. W. Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J. Comp. Neurol. 105: 417–537, 1956.
 60. Blackstad, T. W., K. Brink, J. Hem, and B. Jeune. Distribution of hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods. J. Comp. Neurol. 138: 433–450, 1970.
 61. Braak, H. Zur Pigmentarchitektonik der Grosshirnrinde des Menschen. I. Regio entorhinalis. Z. Zellforsch. Mikrosk. Anat. 127: 407–438, 1972.
 62. Braak, H. Zur Pigmentarchitektonik der Grosshirnrinde des Menschen. II. Subiculum. Z. Zellforsch. Mikrosk. Anat. 131: 235–254, 1972.
 63. Braak, H. On the structure of the human archicortex. I. The cornu ammonis. A Golgi and pigmentarchitectonic study. Cell Tissue Res. 152: 349–383, 1974.
 64. Braak, H. Pigment architecture of the human telencephalic cortex. III. Regio praesubicularis. Cell Tissue Res. 190: 509–523, 1978.
 65. Braak, H., and E. Braak. Neuronal types in the basolateral amygdaloid nuclei of man. Brain Res. Bull. 11: 349–365, 1983.
 66. Briggs, T. L., and W. W. Kaelber. Efferent fiber connections of the dorsal and deep tegmental nuclei of Gudden. An experimental study in the cat. Brain Res. 29: 17–29, 1971.
 67. Brion, S. Korsakoff's syndrome: clinico‐anatomical and physiopathological considerations. In: The Pathology of Memory, edited by G. A. Talland, and N. C. Waugh. New York: Academic, 1969, p. 29–106.
 68. Brockhaus, H. Zur normalen und pathologischen Anatomiedes Mandelkeingebietes. J. Psychol. Neurol. 49: 1–136, 1938.
 69. Brodmann, K. Vergleichende Lokalisationslehre der Grosshirnrinde. Leipzig, Germany: Barth, 1909.
 70. Brown, M. W., and M. D. Cassell. Estimates of the number of neurones in human hippocampus (Abstract). J. Physiol. Lond. 58P, 1980.
 71. Bruce, C., R. Desimone, and C. G. Gross. Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J. Neurophysiol. 46: 369–384, 1981.
 72. Brun, A. An overview of light and electron microscopic changes. In: Alzheimer's Disease, edited by B. Reisberg. New York: Free Press, 1983, p. 37–47.
 73. Brun, A., and L. Gustafson. Distribution of cerebral degeneration in Alzheimer's disease. Arch. Psychiatr. Nervenkr. 223: 15–33, 1976.
 74. Brun, A., and L. Gustafson. Limbic lobe involvement in presenile dementia. Arch. Psychiatr. Nervenkr. 226: 79–93, 1978.
 75. Brust‐Carmona, H., F. J. Alvarez‐Leefmans, and L. Arditti. Differential projections of septal nuclei to ventral and dorsal hippocampus in rabbits. Exp. Neurol. 40: 553–566, 1973.
 76. Buijs, R. M. Immunocytochemical demonstration of vasopressin and oxytocin in the rat brain by light and electron microscopy. J. Histochem. Cytochem. 28: 357–360, 1980.
 77. Buijs, R. M., and D. F. Swaab. Immuno‐electron microscopical demonstration of vasopressin and oxytocin synapses in the limbic system of the rat. Cell Tissue Res. 204: 355–365, 1979.
 78. Burger, P. C. The limbic system in Alzheimer's disease. In: Banbury Report. Biological Aspects of Alzheimer's Disease, edited by R. Katzman. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1983, vol. 15, p. 37–44.
 79. Buser, P., and J. Bancaud. Unilateral connections between amygdala and hippocampus in man. A study of epileptic patients with depth electrodes. Electroencephalogr. Clin. Neurophysiol. 55: 1–12, 1983.
 80. Butcher, L. L., and N. J. Woolf. Cholinergic and serotonergic systems in the brain and spinal cord: anatomic organization, role in intercellular communication processes, and interactive mechanisms. In: Progress in Brain Research. Chemical Transmission in the Brain, edited by R. M. Buijs, R. Pevét, and D. F. Swaab. Amsterdam: Elsevier, 1982, vol. 55, p. 1–40.
 81. Carlsen, J., L. Záborszky, and L. Heimer. Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J. Comp. Neurol. 234: 155–167, 1985.
 82. Carpenter, M. B., K. Nakano, and R. Kim. Nigrothalamic projections in the monkey demonstrated by autoradiographic technics. J. Comp. Neurol. 165: 401–416, 1976.
 83. Cavada, C., and F. Reinoso‐Suarez. Afferent connections of area 20 in the cat studied by means of the retrograde axonal transport of horseradish peroxidase. Brain Res. 270: 319–324, 1983.
 84. Cechetto, D. F., J. Ciriello, and F. R. Calaresu. Afferent connections to cardiovascular sites in the amygdala: a horse‐radish peroxidase study in the cat. J. Auton. Nerv. Syst. 8: 97–110, 1983.
 85. Chan‐Palay, V., C. Köhler, U. Haesler, W. Lang, and G. Yasargil. Distribution of neurons and axons immunoreactive with antisera against neuropeptide Y in the normal human hippocampus. J. Comp. Neurol. 248: 360–375, 1986.
 86. Chan‐Palay, V., W. Lang, U. Haesler, C. Köhler, and G. Yasargil. Distribution of altered hippocampal neurons and axons immunoreactive with antisera against neuropeptide Y in Alzheimer's‐type dementia. J. Comp. Neurol. 248: 376–394, 1986.
 87. Chronister, R. B., G. C. Palmer, J. F. Defrance, R. W. Sikes, and J. I. Hubbard. Histamine: correlative studies in nucleus accumbens. J. Neurobiol. 13: 23–37, 1982.
 88. Chronister, R. B., R. W. Sikes, and L. E. White, Jr. Postcommissural fornix: origin and distribution in the rodent. Neurosci. Lett. 1: 199–202, 1975.
 89. Civelli, O., N. Birnberg, and E. Herbert. Detection and quantitation of pro‐opiomelanocortin mRNA in pituitary and brain tissues from different species. J. Biol. Chem. 257: 6783–6787, 1982.
 90. Claiborne, B. J., D. G. Amaral, and W. M. Cowan. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J. Comp. Neurol. 246: 435–458, 1986.
 91. Cohen, N. J., and L. R. Squire. Preserved learning and retention of pattern analyzing skill in amnesia: dissociation of knowing how and knowing that. Science Wash. DC 210: 207–209, 1980.
 92. Conlon, J. M., W. K. Samson, R. E. Dobbs, L. Orci, and R. H. Unger. Glucagon‐like polypeptides in canine brain. Diabetes 28: 700–702, 1979.
 93. Conrad, L. C. A., C. M. Leonard, and D. W. Pfaff. Connections of the median and dorsal raphe nuclei in the rat: an autoradiographic and degeneration study. J. Comp. Neurol. 156: 179–206, 1974.
 94. Conrad, L. C., and D. W. Pfaff. Autoradiographic tracing of nucleus accumbens efferents in the rat. Brain Res. 113: 589–596, 1976.
 95. Contestabile, A., and B. A. Flumerfelt. Afferent connections of the interpenduncular nucleus and the topographic organization of the habenulo‐interpeduncular pathway: an HRP study in the rat. J. Comp. Neurol. 196: 253–270, 1981.
 96. Corrigall, W. A. Opiates and the hippocampus: a review of the functional and morphological evidence. Pharmacol. Biochem. Behav. 18: 255–262, 1983.
 97. Corsellis, J. A. N. The limbic areas in Alzheimer's disease and in other conditions associated with dementia. In: Alzheimer's Disease, edited by G. E. W. Wolstenholme and M. O'Connor. London: Churchill, 1970, p. 37–50. (Ciba Found. Symp.).
 98. Cowan, W. M., G. Raisman, and T. P. S. Powell. The connexions of the amygdala. J. Neurol. Neuorsurg. Psychiatry 28: 137–151, 1965.
 99. Cowey, A. Sensory and non‐sensory visual disorders in man and monkey. Philos. Trans. R. Soc. Lond. B Biol. Sci. 298: 3–13, 1982.
 100. Crosby, E. C., and T. Humphrey. Studies of the vertebrate telencephalon. II. The nuclear pattern of the anterior olfactory nucleus, tuberculum olfactorium and the amygdaloid complex in adult man. J. Comp. Neurol. 74: 309–352, 1941.
 101. Crosby, E. C., and T. Humphrey. Studies of the vertebrate telencephalon. III. The amygdaloid complex in the shrew. J. Comp. Neurol. 81: 285–305, 1944.
 102. Cruce, J. A. An autoradiographic study of the projections of the mammillothalamic tract in the rat. Brain Res. 37: 21–51, 1975.
 103. Cruce, J. A. An autoradiographic study of the descending connections of the mammillary nuclei of the rat. Brain Res. 85: 211–219, 1977.
 104. Cuello, A. C., and I. Kanazawa. The distribution of substance P immunoreactive fibers in the rat central nervous system. J. Comp. Neurol. 178: 129–156, 1978.
 105. Cummings, J. L., Y. Tomiyasu, S. Read, and D. F. Benson. Amnesia with hippocampal lesions after cardiopulmonary arrest. Neurology 34: 679–681, 1984.
 106. Cummings, S., R. Elde, J. Ells, and A. Lindall. Corticotropin‐releasing factor immunoreactivity is widely distributed within the central nervous system of the rat: an immunohistochemical study. J. Neurosci. 3: 1355–1368, 1983.
 107. Dafny, N., G. Dauth, and S. Gilman. A direct input from amygdaloid complex to caudate nucleus of the rat. Exp. Brain Res. 23: 203–210, 1975.
 108. Daitz, H. M., and T. P. S. Powell. Studies of the connexions of the fornix system. J. Neurol. Neurosurg. Psychiatry 17: 75–82, 1954.
 109. Dam, A. M. The density of neurons in the human hippocampus. Neuropathol. Appl. Neurobiol. 5: 249–264, 1979.
 110. Damasio, A. R. Prosopagnosia. Trends Neurosci. 8: 132–135, 1985.
 111. Danscher, G., E. J. Fjerdingstad, E. Fjerdingstad, and K. Fredens. Heavy metal content in subdivisions of the rat hippocampus (zinc, lead and copper). Brain Res. 112: 442–446, 1976.
 112. Davies, P. Neurotransmitters and neuropeptides in Alzheimer's disease. In: Banbury Report. Biological Aspects of Alzheimer's Disease, edited by R. Katzman. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1983, vol. 15, p. 255–265.
 113. Davies, P., R. Katzman, and R. D. Terry. Reduced somatostatin‐like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementia. Nature Lond. 288: 279–280, 1980.
 114. Davies, P., and R. D. Terry. Cortical somatostatin‐like immunoreactivity in cases of Alzheimer's disease and senile dementia of the Alzheimer type. Neurobiol. Aging 2: 9–14, 1981.
 115. Deacon, T. W., H. Eichenbaum, P. Rosenberg, and K. W. Eckmann. Afferent connections of the perirhinal cortex in the rat. J. Comp. Neurol. 220: 168–190, 1983.
 116. Demeter, S., D. L. Rosene, and G. W. Van Hoesen. Interhemispheric pathways of the hippocampal formation, presubiculum, and entorhinal and posterior parahippocampal cortices in the rhesus monkey: the structure and organization of the hippocampal commissures. J. Comp. Neurol. 233: 30–47, 1985.
 117. De Renzi, E. Memory disorders following focal neocortical damage. Trans. R. Soc. Lond. B 298: 73–83, 1982.
 118. De Renzi, E., P. Faglioni, and P. Villa. Topographical amnesia. J. Neurol. Neurosurg. Psychiatry 40: 498–505, 1977.
 119. Desimone, R., and C. G. Gross. Visual areas in the temporal cortex of the macaque. Brain Res. 178: 363–380, 1979.
 120. Devaney, K. O., and H. A. Johnson. Changes in cell density within the human hippocampal formation as a function of age. Gerontology 30: 100–108, 1984.
 121. De Wied, D. Biobehavioral actions of neurohypophysial peptides. Proc. R. Soc. Lond. B Biol. Sci. 210: 183–195, 1980.
 122. Dogterom, J., T. B. Van Wimersma Greidanus, and D. F. Swaab. Evidence for the release of vasopressin and oxytocin into cerebrospinal fluid: measurements in plasma and CSF of intact and hypophysectomized rats. Neuroendocrinology 24: 108–118, 1977.
 123. Domesick, V. B. Thalamic relationships of the medial cortex in the rat. Brain Behav. Evol. 6: 457–483, 1972.
 124. Dorsa, D. M., F. M. Petracca, D. G. Baskin, and L. E. Cornett. Localization and characterization of vasopressinbinding sites in the amygdala of the rat brain. J. Neurosci. 4: 1764–1770, 1984.
 125. Druga, R. Cortico‐claustral connections. I. Fronto‐claustral connections. Folia Morphol. Prague 14: 391–399, 1966.
 126. Druga, R. Cortico‐claustral connections. II. Connections from the parietal, temporal and occipital cortex to the claustrum. Folia Morphol. Prague 16: 143–149, 1968.
 127. Druga, R. Neocortical projections to the amygdala (an experimental study with the Nauta method). J. Hirnforsch. 11: 467–476, 1970.
 128. Druga, R. Claustro‐neocortical connections in the cat and rat demonstrated by HRP tracing technique. J. Hirnforsch. 23: 191–202, 1982.
 129. Duyckaerts, C., C. Derouesne, J. L. Signoret, F. Gray, R. Escourolle, and P. Castaigne. Bilateral and limited amygdalohippocampal lesions causing a pure amnesic syndrome. Ann. Neurol. 18: 314–319, 1985.
 130. Edinger, E. M., S. Z. Kramer, S. Weiner, P. F. Krayniak, and A. Siegel. The subicular cortex of the cat: an anatomical and electrophysiological study. Exp. Neurol. 63: 504–526, 1979.
 131. Emson, P. C., R. Corder, S. J. Ratter, S. Tomlin, P. J. Lowry, L. H. Ress, A. Arregui, and M. N. Rosser. Regional distribution of pro‐opiomelanocortin‐derived peptides in the human brain. Neuroendocrinology 38: 45–50, 1984.
 132. Emson, P. C., J. F. Rehfeld, and M. N. Rossor. Distribution of cholecystokinin‐like peptides in the human brain. J. Neurochem. 38: 1177–1179, 1982.
 133. Epelbaum, J., M. Ruberg, E. Moyse, F. Javoy‐Agid, B. Dubois, and Y. Agid. Somatostatin and dementia in Parkinson's disease. Brain Res. 278: 376–379, 1983.
 134. Fallon, J. H. Histochemical characterization of dopaminergic, noradrenergic and serotonergic projections to the amygdala. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 175–183.
 135. Fallon, J. H. The islands of Calleja complex of rat basal forebrain. II. Connections of medium and large sized cells. Brain Res. Bull. 10: 775–793, 1983.
 136. Fallon, J. H., and Y. Ben‐Ari. Chairmen's comments. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 151–162.
 137. Fallon, J. H., R. Hicks, and S. E. Loughlin. The origin of cholecystokinin terminals in the basal forebrain of the rat: evidence from immunofluorescence and retrograde tracing. Neurosci. Lett. 37: 29–35, 1983.
 138. Feldman, S. C., C. F. Dreyfus, and E. S. Lichtenstein. Somatostatin neurons in the rodent hippocampus: an in vitro and in vivo immunocytochemical study. Neurosci. Lett. 33: 29–34, 1982.
 139. Fellmann, E., C. Bugnon, and A. Gouget. Immunocytochemical demonstration of corticoliberin‐like immunoreactivity (CLI) in neurones of the rat amygdala central nucleus (ACN). Neurosci. Lett. 34: 253–258, 1982.
 140. Fibiger, H. C. The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res. Rev. 4: 327–388, 1982.
 141. Finch, D. M., and T. L. Babb. Demonstration of caudally directed hippocampal efferents in the rat by intracellular injection of horseradish peroxidase. Brain Res. 214: 405–410, 1981.
 142. Finch, D. M., N. L. Nowlin, and T. L. Babb. Demonstration of axonal projections of neurons in the rat hippocampus and subiculum by intracellular injection of HRP. Brain Res. 271: 201–216, 1983.
 143. Finley, J. C., J. L. Maderdrut, and P. Petrusz. The immunocytochemical localization of enkephalin in the central nervous system of the rat. J. Comp. Neurol. 198: 541–565, 1981.
 144. Fonnum, F. Topographical and subcellular localization of choline acetyltransferase in rat hippocampal region. J. Neurochem. 17: 1029–1037, 1970.
 145. Fonnum, F. Glutamate: a neurotransmitter in mammalian brain. J. Neurochem. 42: 1–11, 1984.
 146. Fonnum, R., R. L. Karlsen, D. M. Sorenssen, K. K. Skrede, and I. Walaas. Localization of neurotransmitters, particularly glutamate, in hippocampus, septum, nucleus accumbens and superior colliculus. In: Progress in Brain Research. Development and Chemical Specificity of Neurons, edited by M. Cuénod, G. W. Kreutzberg, and F. E. Bloom. Amsterdam: Elsevier, 1979, vol. 51, p. 167–191.
 147. Fox, C. A. Certain basal telecephalic centers in the cat. J. Comp. Neurol. 72: 1–62, 1940.
 148. Fox, C. A. Amygdalo‐thalamic connections in Macaca mulatta. Anat. Rec. 103: 537–538, 1949.
 149. Fricke, R., and W. M. Cowan. An autoradiographic study of the commissural and ipsilateral hippocampo‐dentate projections in the adult rat. J. Comp. Neurol. 181: 253–269, 1978.
 150. Frotscher, M., and C. Léránth. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J. Comp. Neurol. 239: 237–246, 1985.
 151. Frotscher, M., C. S. Léránth, K. Lübbers, and W. H. Oertel. Commissural afferents innervate glutamate decarboxylase immunoreactive non‐pyramidal neurons in the guinea pig hippocampus. Neurosci. Lett. 46: 137–143, 1984.
 152. Frotscher, M., and J. Zimmer. Commissural fibers terminate on non‐pyramidal neurons in the guinea pig hippocampus—a combined Golgi/EM degeneration study. Brain Res. 265: 289–293, 1983.
 153. Gaarskjaer, F. B. Organization of the mossy fiber system of the rat studied in extended hippocampi. I. Terminal area related to number of granule and pyramidal cells. J. Comp. Neurol. 178: 49–72, 1978.
 154. Gaarskjaer, F. B. The hippocampal mossy fiber system of the rat studied with retrograde tracing techniques. Correlation between topographic organization and neurogenetic gradients. J. Comp. Neurol. 203: 717–735, 1981.
 155. Gage, F. H., and R. G. Thompson. Differential distribution of norepinephrine and serotonin along the dorsal‐ventral axis of the hippocampal formation. Brain Res. Bull. 5: 771–773, 1980.
 156. Gall, C. The distribution of cholecystokinin‐like immunoreactivity in the hippocampal formation of the guinea pig: localization in the mossy fibers. Brain Res. 306: 73–83, 1984.
 157. Gall, C., N. Brecha, H. J. Karten, and K. J. Chang. Localization of enkephalin‐like immunoreactivity to identified axonal and neuronal populations of the rat hippocampus. J. Comp. Neurol. 198: 335–350, 1981.
 158. Gall, C., and L. Selawski. Supramammillary afferents to guinea pig hippocampus contain substance P‐like immunoreactivity. Neurosci. Lett. 51: 171–176, 1984.
 159. Gaudreau, P., R. Quirion, S. St. Pierre, and C. B. Pert. Characterization and visualization of cholecystokinin receptors in rat brain using [3H]pentagastrin. Peptides Fayetteville 4: 755–762, 1983.
 160. Gee, C. E., C. L. Chen, J. L. Roberts, R. Thompson, and S. J. Watson. Identification of proopiomelanocortin neurones in rat hypothalamus by in situ cDNA‐mRNA hybridisation. Nature Lond. 306: 374–376, 1983.
 161. Geneser‐Jensen, F. A., and T. W. Blackstad. Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig. Z. Zellforsch. Mikrosk. Anat. 114: 460–481, 1971.
 162. Gertz, S. D., R. Lindenberg, and G. W. Piavis. Structural variations in the rostral human hippocampus. Johns Hopkins Med. J. 130: 367–376, 1972.
 163. Ghatei, M. A., S. R. Bloom, H. Langevin, G. P. McGregor, Y. C. Lee, T. E. Adrian, D. J. O'Shaughnessy, and M. A. Blank. Regional distribution of bombesin and seven other regulatory peptides in the human brain. Brain Res. 293: 101–109, 1984.
 164. Gloor, P., A. Olivier, and L. F. Quesney. The role of the amygdala in the expression of psychic phenomena in temporal lobe seizures. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 489–498.
 165. Goldman‐Rakic, P. S., L. D. Selemon, and M. L. Schwartz. Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 12: 719–743, 1984.
 166. Gong, J. Direct connections between hypothalamus and lumbar spinal cord in rabbits. Sci. Sin. 27: 789–799, 1984.
 167. Gottlieb, D. I., and W. M. Cowan. Autoradiographic studies of the commissural and ipsilateral association connections of the hippocampus and dentate gyrus of the rat. J. Comp. Neurol. 149: 393–420, 1973.
 168. Gray, T. S. The morphology of somatostatin‐immunoreactive neurons in the lateral nucleus of the rat amygdala. Peptides Fayetteville 4: 663–668, 1983.
 169. Gray, T. S., M. D. Cassell, and J. Z. Kiss. Distribution of pro‐opiomelanocortin‐derived peptides and enkephalins in the rat central nucleus of the amygdala. Brain Res. 306: 354–358, 1984.
 170. Gray, T. S., M. D. Cassell, G. Nilaver, E. A. Zimmerman, and T. H. Williams. The distribution and ultrastructure of VIP‐immunoreactivity in the central nucleus of the rat amygdala. Neuroscience 11: 399–408, 1984.
 171. Gray, T. S., M. D. Cassell, and T. H. Williams. Synaptology of three peptidergic neuron types in the central nucleus of the rat amygdala. Peptides Fayetteville 3: 273–281, 1982.
 172. Green, J. D. The hippocampus. In: Handbook of Physiology. Neurophysiology, edited by H. W. Magoun. Washington, DC: Am. Physiol. Soc., 1960, vol. II, chapt. 56, p. 1373–1389.
 173. Greenwood, R. S., S. E. Godar, T. A. Reaves, and J. N. Hayward. Cholecystokinin in hippocampal pathways. J. Comp. Neurol. 203: 335–350, 1981.
 174. Groenewegen, H. J., P. Room, M. P. Witter, and A. H. M. Lohman. Cortical afferents of the nucleus accumbens in the cat, studied with anterograde and retrograde transport techniques. Neuroscience 7: 977–995, 1982.
 175. Gudden, H. Klinische und anatomische Beitrage zur Kenntnis der multiplen Alkohol‐neuritis nebst Bemerkungen über Regenerationsvorgange im peripheren Nervensystem. Arch. Psychiatr. Nervenkr. 28: 643–741, 1896.
 176. Guildin, W. O., and H. J. Markowitsch. Cortical and thalamic afferent connections of the insular and adjacent cortex of the cat. J. Comp. Neurol. 229: 393–418, 1984.
 177. Guillery, R. W. A quantitative study of the mamillary bodies and their connections. J. Anat. 89: 19–32, 1955.
 178. Guillery, R. W. Degeneration in the post‐commissural fornix and the mamillary penduncle of the rat. J. Anat. 90: 350–370, 1956.
 179. Haber, S., and R. Elde. The distribution of enkephalin immunoreactive fibers and terminals in the monkey central nervous system: an immunohistochemical study. Neuroscience 7: 1049–1095, 1982.
 180. Haglund, L., L. W. Swanson, and C. Köhler. The projection of the supramammillary nucleus to the hippocampal formation: an immunohistochemical and anterograde transport study with the lectin PHA‐L in the rat. J. Comp. Neurol. 229: 171–185, 1984.
 181. Haines, D. E., and E. Dietrichs. An HRP study of hypothalamocerebellar and cerebello‐hypothalamic connections in squirrel monkey. J. Comp. Neurol. 229: 559–575, 1984.
 182. Hall, E. Some aspects of the structural organization of the amygdala. In: The Neurobiology of the Amygdala, edited by B. E. Eleftheriou. New York: Plenum, 1972, p. 95–121.
 183. Halpain, S., C. M. Wieczorek, and T. C. Rainbow. Localization of l‐glutamate receptors in rat brain by quantitative autoradiography. J. Neurosci. 4: 2247–2258, 1984.
 184. Handelmann, G. E., M. C. Beinfeld, T. L. O'Donohue, J. B. Nelson, and D. E. Brenneman. Extra‐hippocampal projections of CCK neurons of the hippocampus and subiculum. Peptides Fayetteville 4: 331–334, 1983.
 185. Harley, C. W., J. C. Lacaille, and M. Galway. Hypothalamic afferents to the dorsal dentate gyrus contain acetylcholinesterase. Brain Res. 270: 335–339, 1983.
 186. Harris, K. M., P. E. Marshall, and D. M. D. Landis. Ultrastructural study of cholecystokinin‐immunoreactive cells and processes in area CA1 of the rat hippocampus. J. Comp. Neurol. 233: 147–158, 1985.
 187. Hartgraves, S. L., P. L. Mensah, and P. H. Kelly. Regional decreases of cortical choline acetyltransferase after lesions of the septal area and in the area of nucleus basalis magnocellularis. Neuroscience 7: 2369–2376, 1982.
 188. Harting, J. K., W. C. Hall, and I. T. Diamond. Evolution of the pulvinar. Brain Behav. Evol. 6: 424–452, 1972.
 189. Harting, J. K., M. F. Huerta, A. J. Frankfurter, N. L. Strominger, and G. J. Royce. Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. J. Comp. Neurol. 192: 853–882, 1980.
 190. Hayakawa, T., and K. Zyo. Comparative cytoarchitectonic study of Gudden's tegmental nuclei in some mammals. J. Comp. Neurol. 216: 233–234, 1983.
 191. Hayakawa, T., and K. Zyo. Comparative anatomical study of the tegmentomammillary projections in some mammals: a horseradish peroxidase study. Brain Res. 300: 335–349, 1984.
 192. Heath, C. J., and E. G. Jones. The anatomical organization of the suprasylvian gyrus of the cat. Ergeb. Anat. Entwicklungsgesch. 45: 1–64, 1971.
 193. Heimer, L. The olfactory connections of the diencephalon in the rat. Brain Behav. Evol. 6: 484–523, 1972.
 194. Henke, H., and W. Lang. Cholinergic enzymes in neocortex, hippocampus and basal forebrain of non‐neurological and senile dementia of Alzheimer‐type patients. Brain Res. 267: 281–291, 1983.
 195. Herkenham, M. The connections of the nucleus reuniens thalami: evidence for a direct thalamo‐hippocampal pathway in the rat. J. Comp. Neurol. 177: 589–610, 1978.
 196. Herkenham, M., and W. J. Nauta. Efferent connections of the habenular nuclei in the rat. J. Comp. Neurol. 187: 19–47, 1979.
 197. Herzog, A. G., and T. L. Kemper. Amygdaloid changes in aging and dementia. Arch. Neurol. 37: 625–629, 1980.
 198. Herzog, A. G., and G. W. Van Hoesen. Temporal neocortical afferent connections to the amygdala in the rhesus monkey. Brain Res. 115: 57–69, 1976.
 199. Higgins, G. A., and J. S. Schwaber. Somatostatinergic projections from the central nucleus of the amygdala to the vagal nuclei. Peptides Fayetteville 4: 657–662, 1983.
 200. Hjorth‐Simonsen, A. Hippocampal efferents to the ipsilateral entorhinal area: an experimental study in the rat. J. Comp. Neurol. 142: 417–437, 1971.
 201. Hjorth‐Simonsen, A. Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J. Comp. Neurol. 146: 219–231, 1972.
 202. Hjorth‐Simonsen, A. Some intrinsic connections of the hippocampus in the rat: an experimental analysis. J. Comp. Neurol. 147: 145–161, 1973.
 203. Hjorth‐Simonsen, A. Distribution of commissural afferents to the hippocampus of the rabbit. J. Comp. Neurol. 176: 495–514, 1977.
 204. Hjorth‐Simonsen, A., and B. Jeune. Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144: 215–231, 1972.
 205. Hjorth‐Simonsen, A., and S. Laurberg. Commissural connections of the dentate area of the rat. J. Comp. Neurol. 174: 591–606, 1977.
 206. Hoffman, D. W. Effects of chemical and surgical lesions on levels of chromatographically identified enkephalin‐like peptides in rat hippocampus. Brain Res. 310: 7–12, 1984.
 207. Hoffman, D. W., R. A. Altschuler, and J. Gutierrez. Multiple molecular forms of enkephalins in the guinea pig hippocampus. J. Neurochem. 41: 1641–1647, 1983.
 208. Hoffman, D. W., and N. Zamir. Localization and quantitation of dynorphin B in the rat hippocampus. Brain Res. 324: 354–357, 1984.
 209. Hökfelt, T., K. Fuxe, O. Johansson, and A. Ljungdahl. Pharmacohistochemical evidence of the existence of dopamine nerve terminals in the limbic cortex. Eur. J. Pharmacol. 25: 108–112, 1974.
 210. Hökfelt, T., J. F. Rehfeld, L. Skirboll, B. Ivemark, M. Goldstein, and K. Markey. Evidence for coexistence of dopamine and CCK in meso‐limbic neurones. Nature Lond. 285: 476–478, 1980.
 211. Holmes, E. J., N. Butters, S. Jacobson, and B. M. Stein. An examination of the effects of mammillary‐body lesions on reversal learning sets in monkeys. Physiol. Psychol. 11: 159–165, 1983.
 212. Holmes, E. J., S. Jacobson, B. M. Stein, and N. Butters. Ablations of the mammillary nuclei in monkeys: effects on postoperative memory. Exp. Neurol. 81: 97–113, 1983.
 213. Holstege, G., L. Meiners, and K. Tan. Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons, and medulla oblongata in the cat. Exp. Brain Res. 58: 379–391, 1985.
 214. Hooper, M. W., and F. Vogel. The limbic system in Alzheimer's disease. Am. J. Pathol. 85: 1–21, 1976.
 215. Hoover, D. B., E. A. Muth, and D. M. Jacobowitz. A mapping of the distribution of acetylcholine, choline acetyltransferase and acetylcholinesterase in discrete areas of rat brain. Brain Res. 153: 259–306, 1978.
 216. Hopkins, D. A. Amygdalotegmental projections in the rat, cat and rhesus monkey. Neurosci. Lett. 1: 263–270, 1975.
 217. Hopkins, D. A., and G. Holstege. Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Exp. Brain Res. 32: 529–547, 1978.
 218. Hopkins, D. A., J. H. McLean, and Y. Takeuchi. Amygdalotegmental projections: light and electron microscope studies utilizing anterograde degeneration and the anterograde and retrograde transport of horseradish peroxidase (HRP). In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 133–147.
 219. Horel, J. The neuroanatomy of amnesia: a critique of the hippocampal memory hypothesis. Brain 101: 403–445, 1978.
 220. Horel, J. A., and L. J. Misantone. The Klüver‐Bucy syndrome produced by partial isolation of the temporal lobe. Exp. Neurol. 42: 101–112, 1974.
 221. Horel, J. A., and L. J. Misantone. Visual discrimination impaired by cutting temporal lobe connections. Science Wash. DC 193: 336–338, 1976.
 222. Houser, C. R., G. D. Crawford, R. P. Barber, P. M. Salvaterra, and J. E. Vaughn. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res. 266: 97–119, 1983.
 223. Hyman, B. T., G. W. Van Hoesen, A. R. Damasio, and C. L. Barnes. Alzheimer's disease: cell‐specific pathology isolates the hippocampal formation. Science Wash. DC 225: 1168–1170, 1984.
 224. Ilinsky, I. A., M. L. Jouandet, and P. S. Goldman‐Rakic. Organization of the nigrothalamocortical system in the rhesus monkey. J. Comp. Neurol. 236: 315–330, 1985.
 225. Imamura, K., N. Onoda, and S. F. Takagi. Odor response characteristics of thalamic mediodorsal nucleus neurons in the rabbit. Jpn. J. Physiol. 34: 55–73, 1984.
 226. Inagaki, S., Y. Kawai, T. Matsuzaki, S. Shiosaka, and M. Tohyama. Precise terminal fields of the descending somatostatinergic neuron system from the amygdaloid complex of the rat. J. Hirnforsch. 24: 345–356, 1983.
 227. Inagaki, S., Y. Kubota, K. Shinoda, Y. Kawai, and M. Tohyama. Neurotensin‐containing pathway from the endopiriform nucleus and the adjacent prepiriform cortex to the dorsomedial thalamic nucleus in the rat. Brain Res. 260: 143–146, 1983.
 228. Insausti, R., D. G. Amaral, and W. M. Cowan. The monkey entorhinal cortex. II. Cortical afferents. J. Comp. Neurol. In press.
 229. Insausti, R., D. G. Amaral, and W. M. Cowan. The monkey entorhinal cortex. III. Subcortical afferents. J. Comp. Neurol. In press.
 230. Irle, E., and H. J. Markowitsch. Connections of the hippocampal formation, mamillary bodies, anterior thalamus and cingulate cortex. Exp. Brain Res. 47: 79–94, 1982.
 231. Irle, E., and H. J. Markowitsch. Thiamine deficiency in the cat leads to severe learning deficits and to widespread neuroanatomical damage. Exp. Brain Res. 48: 199–208, 1982.
 232. Irle, E., and H. J. Markowitsch. Single and combined lesions of the cat's mediodorsal nucleus and the mamillary bodies lead to severe deficits in the acquisition of an alternation task. Behav. Brain Res. 6: 147–165, 1982.
 233. Irle, E., and H. J. Markowitsch. Widespread cortical projections of the hippocampal formation in the cat. Neuroscience 7: 2637–2647, 1982.
 234. Irle, E., and H. J. Markowitsch, and M. Streicher. Cortical and subcortical, including sensory‐related, afferents to the thalamic mediodorsal nucleus of the cat. J. Hirnforsch. 25: 29–51, 1984.
 235. Irle, E., M. Sarter, W. O. Guldin, and H. J. Markowitsch. Afferents to the ventral tegmental nucleus of Gudden in the mouse, rat, and cat. J. Comp. Neurol. 228: 509–541, 1984.
 236. Ishikawa, I., S. Kawamura, and O. Tanaka. An experimental study on the efferent connections on the amygdaloid complex in the cat. Acta Med. Okayama 23: 519–539, 1969.
 237. Isseroff, A., H. E. Rosvold, T. W. Galkin, and P. S. Goldman‐Rakic. Spatial memory impairments following damage to the mediodorsal nucleus of the thalamus in rhesus monkeys. Brain Res. 232: 97–113, 1982.
 238. Jackson, J. C., and R. M. Benjamin. Unit discharges in the mediodorsal nucleus of the rabbit evoked by electrical stimulation of the olfactory bulb. Brain Res. 75: 193–201, 1974.
 239. Jackson, J. C., G. T. Golden, and R. M. Benjamin. The distribution of olfactory input in the opossum mediodorsal nucleus. Brain Res. 138: 229–240, 1977.
 240. Jacobowitz, D. M., and T. L. O'Donohue. Alpha‐melanocyte stimulating hormone: immunohistochemical identification and mapping in neurons of rat brain. Proc. Natl. Acad. Sci. USA 75: 6300–6304, 1978.
 241. Jacobowitz, D. M., T. L. O'Donohue, W. Y. Chey, and T. M. Chang. Mapping of motilin‐immunoreactive neurons of the rat brain. Peptides Fayetteville 2: 479–487, 1981.
 242. Jacobson, S., N. Butters, and N. J. Tovsky. Afferent and efferent subcortical projections of behaviorally defined sectors of prefrontal granular cortex. Brain Res. 159: 279–296, 1978.
 243. Jacobson, S., and J. Q. Trojanowski. Amygdaloid projections to prefrontal granular cortex in rhesus monkey demonstrated with horseradish peroxidase. Brain Res. 100: 132–139, 1975.
 244. Jamada, M., and P. Mehraein. Verteilungsmuster der senilen Veränderungen im Gehirn. Arch. Psychiatr. Nervenkr. 211: 308–324, 1968.
 245. Jennes, L., and W. E. Stumpf. LHRH‐systems in the brain of the golden hamster. Cell Tissue Res. 209: 239–256, 1980.
 246. Jimenez‐Castellanos, J. The amygdaloid complex in monkey studied by reconstructional methods. J. Comp. Neurol. 91: 506–527.
 247. Jirikowski, G., I. Reisert, C. Pilgrim, and W. H. Oertel. Coexistence of glutamate decarboxylase and somatostatin immunoreactivity in cultured hippocampal neurons of the rat. Neurosci. Lett. 46: 35–39, 1984.
 248. Johansson, O., T. Hökfelt, and R. P. Elde. Immunohistochemical distribution of somatostatin‐like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13: 265–339, 1984.
 249. Johansson, O., T. Hökfelt, R. P. Elde, M. Schultzberg, and L. Terenius. Immunohistochemical distribution of enkephalin neurons. Adv. Biochem. Psychopharmacol. 18: 51–69, 1978.
 250. Johnston, J. B. Further contributions to the study of the evolution of the forebrain. J. Comp. Neurol. 36: 143–192, 1923.
 251. Jones, B., and M. Mishkin. Limbic lesions and the problem of stimulus‐reinforcement associations. Exp. Neurol. 36: 362–377, 1972.
 252. Jones, B. E., and R. Y. Moore. Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study. Brain Res. 127: 23–53, 1977.
 253. Jones, E. G., and H. Burton. A projection from the medial pulvinar to the amygdala in primates. Brain Res. 104: 142–147, 1976.
 254. Jones, E. G., H. Burton, C. B. Saper, and L. W. Swanson. Midbrain, diencephalic and cortical relationships of the basal nucelus of Meynert and associated structures in primates. J. Comp. Neurol. 167: 385–420, 1976.
 255. Jones, E. G., and T. P. S. Powell. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93: 793–820, 1970.
 256. Jürgens, U. Afferent fibers to the cingular vocalization region in the squirrel monkey. Exp. Neurol. 80: 395–409, 1983.
 257. Kaada, B. R. Stimulation and regional ablation of the amygdaloid cortex with reference to functional representations. In: The Neurobiology of the Amygdala, edited by B. E. Eleftheriou. New York: Plenum, 1972, p. 205–282.
 258. Kahn, D., G. M. Abrams, E. A. Zimmerman, R. Carraway, and S. E. Leeman. Neurotensin neurons in the rat hypothalamus: an immunohistochemical study. Endocrinology 107: 47–54, 1980.
 259. Kaitz, S. S., and R. T. Robertson. Thalamic connections with limbic cortex. II. Corticothalamic projections. J. Comp. Neurol. 195: 527–545, 1981.
 260. Kamal, A. M., and T. Tömböl. Olfactory and temporal projections to the amygdala. Verh. Anat. Ges. 70: 283–288, 1976.
 261. Kataoka, Y., K. Shibata, Y. Gomita, and S. Ueki. The mammillary body is a potential site of antianxiety action of benzodiazepines. Brain Res. 241: 374–377, 1982.
 262. Katzman, R. Banbury Report. Biological Aspects of Alzheimer's Disease. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1983, vol. 15.
 263. Kawai, Y., S. Inagaki, S. Shiosaka, E. Senba, Y. Hara, M. Sakanaka, K. Takatsuki, and M. Tohyama. Long descending projections from amygdaloid somatostatin‐containing cells to the lower brain stem. Brain Res. 239: 603–607, 1982.
 264. Kelley, A. E., and V. B. Domesick. The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde‐ and retrograde‐horseradish peroxidase study. Neuroscience 7: 2321–2335, 1982.
 265. Kelley, A. E., V. B. Domesick, and W. J. H. Nauta. The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7: 615–630, 1982.
 266. Kemper, T. L. Senile dementia: a focal disease in the temporal lobe. In: Senile Dementia: A Biomedical Approach, edited by K. Nandy. New York: Elsevier/North‐Holland, 1978, p. 105–113.
 267. Kemper, T. L. Organization of the neuropathology of the amygdala in Alzheimer's disease. In: Banbury Report. Biological Aspects of Alzheimer's Disease, edited by R. Katzman. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1983, vol. 15, p. 31–35.
 268. Kemper, T. Neuroanatomical and neuropathological changes in normal aging and in dementia. In: Clinical Neurology of Aging, edited by M. L. Albert. New York: Oxford Univ. Press, 1984, p. 9–52.
 269. Kievit, J., and H. G. Kuypers. Subcortical afferents to the frontal lobe in the rhesus monkey studied by means of retrograde horseradish peroxidase transport. Brain Res. 85: 261–266, 1975.
 270. Kievit, J., and H. G. J. M. Kuypers. Organization of the thalamo‐cortical connexions to the frontal lobe in the rhesus monkey. Exp. Brain Res. 29: 299–322, 1977.
 271. King, J. C., and E. L. Anthony. LHRH neurons and their projections in humans and other mammals: species comparisons. Peptides Fayetteville 5: 195–207, 1984.
 272. Kiyama, H., S. Shiosaka, K. Takami, K. Tateishi, E. Hashimura, T. Hamaoka, and M. Tohyama. CCK pathway from supramammillary region to the nucleus anterior ventralis thalami of the young rats. Peptides Fayetteville 5: 889–893, 1984.
 273. Kiyama, H., S. Shiosaka, K. Tateishi, E. Hashimura, T. Hamaoka, and M. Tohyama. Cholecystokinin‐8‐like immunoreactive neuron pathway from the supramammillary region to the ventral tegmental nucleus of Gudden of the rat. Brain Res. 304: 397–400, 1984.
 274. Klüver, H., and P. C. Bucy. Preliminary analysis of functions of the temporal lobes in monkeys. Arch. Neurol. Psychiatry 42: 979–1000, 1939.
 275. Knowles, E. D., and P. A. Schwartzkroin. Local circuit synaptic interactions in hippocampal brain slices. J. Neurosci. 1: 318–322, 1981.
 276. Kobayashi, R. M., M. Palkovits, I. J. Kopin, and D. M. Jacobowitz. Biochemical mapping of noradrenergic nerves arising from the rat locus coeruleus. Brain Res. 77: 269–279, 1974.
 277. Koda, L. Y., J. A. Schulman, and F. E. Bloom. Ultrastructural identification of noradrenergic terminals in rat hippocampus: unilateral destruction of the locus coeruleus with 6‐hydroxydopamine. Brain Res. 145: 190–195, 1978.
 278. Köhler, C. Distribution and morphology of vasoactive intestinal polypeptide‐like immunoreactive neurons in regio superior of the rat hippocampal formation. Neurosci. Lett. 33: 265–270, 1982.
 279. Köhler, C. A morphological analysis of vasoactive intestinal polypeptide (VIP)‐like immunoreactive neurons in the area dentata of the rat brain. J. Comp. Neurol. 221: 247–262, 1983.
 280. Köhler, C. Morphological details of the projection from the presubiculum to the entorhinal area as shown with the novel PHA‐L immunohistochemical tracing method in the rat. Neurosci. Lett. 45: 285–290, 1984.
 281. Köhler, C. Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J. Comp. Neurol. 236: 504–522, 1985.
 282. Köhler, C., and V. Chan‐Palay. Gamma‐aminobutyric acid interneurons in the rat hippocampal region studied by retrograde transport of glutamic acid decarboxylase antibody after in vivo injections. Anat. Embryol. 166: 53–66, 1983.
 283. Köhler, C., and V. Chan‐Palay. Distribution of gamma‐aminobutyric acid containing neurons and terminals in the septal area. Anat. Embryol. 167: 53–65, 1983.
 284. Köhler, C., and V. Chan‐Palay. Somatostatin and vasoactive intestinal polypeptide‐like immunoreactive cells and terminals in the retrohippocampal region of the rat brain. Anat. Embryol. 167: 151–172, 1983.
 285. Köhler, C., V. Chan‐Palay, and J. Y. Wu. Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anat. Embryol. 169: 41–44, 1984.
 286. Köhler, C., L. Haglund, and L. W. Swanson. A diffuse alpha‐MSH‐immunoreactive projection to the hippocampus and spinal cord from individual neurons in the lateral hypothalamic area and zona incerta. J. Comp. Neurol. 223: 501–514, 1984.
 287. Köhler, C., M. T. Shipley, B. Srebro, and W. Harkmark. Some retrohippocampal afferents to the entorhinal cortex. Cells of origin as studied by the HRP method in the rat and mouse. Neurosci. Lett. 10: 115–120, 1978.
 288. Köhler, C., and H. Steinbusch. Identification of serotonin and non‐serotonin‐containing neurons of the mid‐brain raphe projecting to the entorhinal area and the hippocampal formation. A combined immunohistochemical and fluorescent retrograde tracing study in the rat brain. Neuroscience 7: 951–975, 1982.
 289. Köhler, C., L. W. Swanson, L. Haglund, and Y. Y. Wu. The cytoarchitecture, histochemistry, and projections of the tuberomammillary nucleus in the rat. Neuroscience 16: 85–110, 1985.
 290. Koikegami, H. Amygdala and other related limbic structures; experimental studies on the anatomy and function. Acta Med. Biol. 10: 161–277, 1963.
 291. Kolliker, A. Handbuch der Gewebelehre der Menschen. Leipzig, Germany: Engelmann, 1896.
 292. Kosel, K. C., G. W. Van Hoesen, and D. L. Rosene. Nonhippocampal cortical projections from the entorhinal cortex in the rat and rhesus monkey. Brain Res. 244: 201–213, 1982.
 293. Kosel, K. C., G. W. Van Hoesen, and D. L. Rosene. A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat. Brain Res. 269: 347–351, 1983.
 294. Kosel, K. C., G. W. Van Hoesen, and J. R. West. Olfactory bulb projections to the parahippocampal area of the rat. J. Comp. Neurol. 198: 467–482, 1981.
 295. Kosmal, A., I. Stepniewska, and G. Markow. Laminar organization of efferent connections of the prefrontal cortex in the dog. Acta Neurobiol. 43: 115–127, 1983.
 296. Krayniak, P. F., S. Weiner, and A. Seigel. An analysis of the efferent connections of the septal area in the cat. Brain Res. 189: 15–29, 1980.
 297. Krettek, J. E., and J. L. Price. A direct input from the amygdala to the thalamus and the cerebral cortex. Brain Res. 67: 169–174, 1974.
 298. Krettek, J. E., and J. L. Price. Projections from the amygdala to the perirhinal and entorhinal cortices and the subiculum. Brain Res. 71: 150–154, 1974.
 299. Krettek, J. E., and J. L. Price. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J. Comp. Neurol. 171: 157–192, 1977.
 300. Krettek, J. E., and J. L. Price. Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J. Comp. Neurol. 172: 687–722, 1977.
 301. Krettek, J. E., and J. L. Price. Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat. J. Comp. Neurol. 172: 723–752, 1977.
 302. Krettek, J. E., and J. L. Price. Amygdaloid piojections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. Comp. Neurol. 178: 225–253, 1978.
 303. Krettek, J. E., and J. L. Price. A description of the amygdaloid complex in the rat and cat with observations on intraamygdaloid axonal connections. J. Comp. Neurol. 178: 255–280, 1978.
 304. Krieckhaus, E. E. The mammillary bodies: their functions and anatomical connections. Acta Biol. Exp. 27: 319–337, 1967.
 305. Krisch, B. Somatostatin‐immunoreactive fiber projections into the brain stem and the spinal cord of the rat. Cell Tissue Res. 217: 531–552, 1981.
 306. Kubek, M. J., J. F. Wilber, and J. E. Leesthma. The identification of gonadotropin‐releasing hormone (GnRH) in hypothalamic and extrahypothalamic loci of the human nervous system. Horm. Metab. Res. 11: 26–29, 1979.
 307. Kunzle, H. Thalamic projections from the precentral motor cortex in Macaca fascicularis. Brain. Res. 105: 253–267, 1976.
 308. Kuypers, H. G. J. M., M. K. Szwarcbart, M. Mishkin, and H. E. Rosvold. Occipitotemporal corticocortical connections in the rhesus monkey. Exp. Neurol. 11: 245–262, 1965.
 309. Laatsch, R. H., and W. M. Cowan. Electron microscopic studies of the rat dentate gyrus. II. Degeneration of commissural afferents. J. Comp. Neurol. 130: 241–262, 1966.
 310. Lauer, E. W. The nuclear pattern and fiber connections of certain basal telencephalic centers in the macaque. J. Comp. Neurol. 82: 215–255, 1945.
 311. Laurberg, S. Commissural and intrinsic connections of the rat hippocampus. J. Comp. Neurol. 184: 685–708, 1979.
 312. Laurberg, S., and K. E. Sørensen. Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3). Brain Res. 212: 287–300, 1981.
 313. Lehman, M. N., and S. S. Winans. Evidence for a ventral non‐strial pathway from the amygdala to the bed nucleus of the stria terminalis in the male golden hamster. Brain Res. 268: 139–146, 1983.
 314. Leichnetz, G. R., and J. Astruc. Efferent connections of the orbitofrontal cortex in the marmoset (Saguinus oedipus). Brain Res. 84: 169–180, 1975.
 315. Leichnetz, G. R., and J. Astruc. Preliminary evidence for a direct projection of the prefrontal cortex to the hippocampus in the squirrel monkey. Brain Behav. Evol. 11: 355–364, 1975.
 316. Leichnetz, G. R., and J. Astruc. The squirrel monkey entorhinal cortex: architecture and medial frontal afferents. Brain Res. Bull. 1: 351–358, 1976.
 317. Leichnetz, G. R., and J. Astruc. The course of some prefrontal corticofugals to the pallidum, substantia innominata, and amygdaloid complex in monkeys. Exp. Neurol. 54: 104–109, 1977.
 318. Leonard, C. M. The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res. 12: 321–343, 1969.
 319. Leonard, C. M. The connections of the dorsomedial nuclei. Brain Behav. Evol. 6: 524–541, 1972.
 320. Léránth, C., M. Frotscher, T. Tömböl, and M. Palkovits. Ultrastructure and synaptic connections of vasoactive intestinal polypeptide‐like immunoreactive non‐pyramidal neurons and axon terminals in the rat hippocampus. Neuroscience 12: 531–542, 1984.
 321. Levay, S., and H. Sherk. The visual claustrum of the cat. I. Structure and connections. J. Neurosci. 1: 956–980, 1981.
 322. LeVay, S., and H. Sherk. The visual claustrum of the cat. II. The visual field map. J. Neurosci. 1: 981–992, 1981.
 323. Lewis, P. R., and C. C. D. Shute. The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra‐optic crest. Brain 90: 521–590, 1967.
 324. Lewis, P. R., C. C. D. Shute, and A. Silver. Confirmation from choline acetylase analyses of a massive cholinergic innervation to the rat hippocampus. J. Physiol. Lond. 191: 215–224, 1967.
 325. Lilly, R., J. L. Cummings, D. F. Benson, and M. Frankel. The human Klüver‐Bucy syndrome. Neurology 33: 1141–1145, 1983.
 326. Lindvall, O., and A. Björklund. The organization of the ascending catecholamine neuron systems in the rat brain. Acta Physiol. Scand. 412: 1–48, 1974.
 327. Liu, R., L. Chang, and G. Wickern. The dorsal tegmental nucleus: an axoplasmic transport study. Brain Res. 310: 123–132, 1984.
 328. Ljungdahl, A., T. Hökfelt, and G. Nilsson. Distribution of substance P‐like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve terminals. Neuroscience 3: 861–943, 1978.
 329. Llamas, A., C. Avendano, and F. Reinoso‐Suarez. Amygdaloid projections to prefrontal and motor cortex. Science Wash. DC 195: 794–797, 1977.
 330. Loewy, A. D., and H. Burton. Nuclei of the solitary tract: efferent connections to the lower brainstem and spinal cord of the cat. J. Comp. Neurol. 181: 421–450, 1978.
 331. Lopes da Silva, F. H., D. E. A. T. Arnolds, and H. C. Neijt. A functional link between the limbic cortex and ventral striatum: physiology of the subiculum accumbens pathway. Exp. Brain Res. 55: 205–214, 1984.
 332. Loren, I., J. Alumets, R. Håkanson, and F. Sundler. Distribution of gastrin and CCK‐like peptides in rat brain. An immunocytochemical study. Histochemistry 59: 249–257, 1979.
 333. Loren, I., P. C. Emson, J. Fahrenkrug, A. Björklund, J. Alumets, R. Håkanson, and F. Sundler. Distribution of vasoactive intestinal polypeptide in rat and mouse brain. Neuroscience 4: 1953–1956, 1979.
 334. Lorente de Nó, R. Studies on the structure of the cerebral cortex. I. The area entorhinalis. J. Psychol. Neurol. 45: 381–438, 1933.
 335. Lorente de Nó, R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 46: 113–177, 1934.
 336. Loughlin, S. E., and J. H. Fallon. Dopaminergic and non‐dopaminergic projections to amygdala from substantia nigra and ventral tegmental area. Brain Res. 262: 334–338, 1983.
 337. Loy, R., D. A. Koziell, J. D. Lindsey, and R. Moore. Noradrenergic innervation of the adult rat hippocampal formation. J. Comp. Neurol. 189: 699–710, 1980.
 338. Luiten, P. G. M., T. Ono, H. Nishijo, and M. Fukuda. Differential input from the amygdaloid body to the ventromedial hypothalamic nucleus in the rat. Neurosci. Lett. 35: 253–258, 1983.
 339. Macchi, G., M. Bentivoglio, D. Miniacchi, and M. Molinari. The organization of the claustroneocortical projections in the cat studied by means of the HRP retrograde axonal transport. J. Comp. Neurol. 195: 681–695, 1981.
 340. Macchi, G., M. Bentivoglio, D. Minciacchi, and M. Molinari. Claustroneocortical projections studied in the cat by means of multiple retrograde fluorescent tracing. J. Comp. Neurol. 215: 121–134, 1983.
 341. Macchi, G., M. Bentivoglio, M. Molinari, and D. Minciacchi. The thalamo‐caudate versus thalamo‐cortical projections as studied in the cat with fluorescent retrograde double labeling. Exp. Brain Res. 54: 225–239, 1984.
 342. Macchi, G., M. Bentivoglio, P. Rossini, and E. Tempesta. The basolateral amygdaloid projections to the neocortex in the cat. Neurosci. Lett. 9: 347–351, 1978.
 343. MacLean, P. D., and D. W. Ploog. Cerebral representation of penile erection. J. Neurophysiol. 25: 29–55, 1962.
 344. Mair, W. G. P., E. K. Warrington, and L. Weiskrantz. Memory disorder in Korsakoff's psychosis. Brain 102: 749–783, 1979.
 345. Malo, P., M. D. Laviña, E. L. Rodriguez Echandia, and A. Machado. Distribution of acetylcholinesterase along the dorso‐ventral axis of the hippocampal formation in the rabbit. J. Neurochem. 29: 729–733, 1977.
 346. Marchand, E. R., J. N. Riley, and R. Y. Moore. Interpeduncular nucleus afferents in the rat. Brain Res. 193: 339–352, 1980.
 347. Markowitsch, H. J. Thalamic mediodorsal nucleus and memory: a critical evaluation of studies in animals and man. Neurosci. Biobehav. Rev. 6: 351–380, 1982.
 348. Markowitsch, H. J. Can amnesia be caused by damage of a single brain structure? Cortex 20: 27–45, 1984.
 349. Markowitsch, H. J., E. Irle, R. Bang‐Olsen, and P. Flindt‐Egebak. Claustral efferents to the cat's limbic cortex studied with retrograde and anterograde tracing techniques. Neuroscience 12: 409–425, 1984.
 350. Markowitsch, H. J., E. Irle, and M. Streicher. The thalamic mediodorsal nucleus receives input from thalamic and cortical regions related to vision. Neurosci. Lett. 32: 131–136, 1982.
 351. Marley, P. D., P. C. Emson, S. P. Hunt, and J. Fahrenkrug. A long ascending projection in the rat brain containing vasoactive intestinal polypeptide. Neurosci. Lett. 27: 261–266, 1981.
 352. Mauguière, F., and C. Baleydier. Topographical organization of medial pulvinar neurons sending fibres to Brodman's areas 7, 21 and 22 in the monkey. Exp. Brain Res. 31: 605–607, 1978.
 353. McBride, R. L., and J. Sutin. Amygdaloid and pontine projections to the ventromedial nucleus of the hypothalamus. J. Comp. Neurol. 174: 377–396, 1977.
 354. McDonald, A. J. Cytoarchitecture of the central amygdaloid nucleus of the rat. J. Comp. Neurol. 208: 401–418, 1982.
 355. McDonald, A. J. Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat. J. Comp. Neurol. 222: 589–606, 1984.
 356. McDuff, T., and S. M. Sumi. Subcortical degeneration in Alzheimer's disease. Neurology 35: 123–126, 1985.
 357. McGinty, J. F., S. J. Henriksen, A. Goldstein, L. Terenius, and F. E. Bloom. Dynorphin is contained with hippocampal mossy fibers: immunochemical alterations after kainic acid administration and colchicine‐induced neurotoxicity. Proc. Natl. Acad. Sci. USA 80: 589–593, 1983.
 358. Meadows, J. C. The anatomical basis of prosopagnosia. J. Neurol. Neurosurg. Psychiatry 37: 489–501, 1974.
 359. Mehler, W. R. Subcortical afferent connections of the amygdala in the monkey. J. Comp. Neurol. 190: 733–762, 1980.
 360. Mehler, W. R., J. K. Pretorius, K. D. Phelan, and P. W. Mantyh. Diencephalic afferent connections of the amygdala in the squirrel monkey with observations and comments on the cat and rat. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 105–120.
 361. Meibach, R. C., and A. Siegel. The origin of fornix fibers which project to the mammillary bodies in the rat: a horseradish peroxidase study. Brain Res. 88: 508–512, 1975.
 362. Meibach, R. C., and A. Siegel. Efferent connections of the septal area in the rat: an analysis utilizing retrograde and anterograde transport methods. Brain Res. 119: 1–20, 1977.
 363. Meibach, R. C., and A. Siegel. Efferent connections of the hippocampal formation in the rat. Brain Res. 124: 197–224, 1977.
 364. Meisenberg, G., and W. H. Simmons. Centrally mediated effects of neurohypophyseal hormones. Neurosci. Biobehav. Rev. 7: 263–280, 1980.
 365. Mellgren, S. I., W. Harkmark, and B. Srebro. Some enzyme histochemical characteristics of the human hippocampus. Cell Tissue Res. 181: 459–471, 1977.
 366. Merchenthaler, I. Corticotropin releasing factor (CRF)‐like immunoreactivity in the rat central nervous system. Extrahypothalamic distribution. Peptides Fayetteville 5: 53–69, 1984.
 367. Mesulam, M. M., and E. J. Mufson. Insula of the old world monkey. I. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain. J. Comp. Neurol. 212: 1–22, 1982.
 368. Mesulam, M. M., and E. J. Mufson. Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107: 253–274, 1984.
 369. Mesulam, M. M., E. J. Mufson, A. I. Levey, and B. H. Wainer. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J. Comp. Neurol. 214: 170–197, 1983.
 370. Mesulam, M. M., E. J. Mufson, A. I. Levey, and B. H. Wainer. Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12: 669–686, 1984.
 371. Miller, A. K. H., R. L. Alston, C. Q. Mountjoy, and J. A. N. Corsellis. Automated differential cell counting on a sector of the normal human hippocampus: the influence of age. Neuropathol. Appl. Neurobiol. 10: 123–141, 1984.
 372. Millhouse, O. E., and J. DeOlmos. Neuronal configurations in lateral and basolateral amygdala. Neuroscience 10: 1269–1300, 1983.
 373. Milner, B. Memory and the medial temporal regions of the brain. In: Biology of Memory, edited by K. H. Pribram and D. E. Broadbent. New York: Academic, 1970, p. 29–50.
 374. Milner, B., and M. Petrides. Behavioural effects of frontallobe lesions in man. Trends Neurosci. 7: 403–407, 1984.
 375. Milner, T. A., and D. G. Amaral. Evidence for a ventral septal projection to the hippocampal formation of the rat. Exp. Brain Res. 55: 579–585, 1984.
 376. Milner, T. A., R. Loy, and D. G. Amaral. An anatomical study of the development of the septo‐hippocampal projection in the rat. Dev. Brain Res. 8: 343–371, 1983.
 377. Mishkin, M. Memory in monkeys severely impaired by combined but not separate removal of amygdala and hippocampus. Nature Lond. 273: 297–298, 1978.
 378. Mishkin, M. A memory system in the monkey. Philos. Trans. R. Soc. Lond. B Biol. Sci. 298: 85–95, 1982.
 379. Mishkin, M., and J. Aggleton. Multiple functional contributions of the amygdala in the monkey. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 409–420.
 380. Mishkin, M., B. Malamut, and J. Bachevalier. Memories and habits: two neural systems. In: Neurobiology of Learning and Memory, edited by G. Lynch, J. L. McGaugh, and N. M. Weinberger. New York: Guilford, 1984, p. 65–77.
 381. Mizuno, N., O. Takahashi, T. Satoda, and R. Matsushima. Amygdaloid projections in the macaque monkey. Neurosci. Lett. 53: 327–330, 1985.
 382. Mizuno, N., K. Uchida, S. Nomura, Y. Nakamura, T. Sugimoto, and M. Uemura‐Sumi. Extrageniculate projections to the visual cortex in the macaque monkey: an HRP study. Brain Res. 212: 454–459, 1981.
 383. Moga, M. M., and T. S. Gray. Evidence for corticotropin‐releasing factor, neurotensin, and somatostatin in the neural pathway from the central nucleus of the amygdala to the parabrachial nucleus. J. Comp. Neurol. 241: 275–284, 1985.
 384. Moore, R. Y., and A. E. Halaris. Hippocampal innervation by serotonin neurons of the midbrain raphe in the rat. J. Comp. Neurol. 164: 171–184, 1975.
 385. Morest, D. K. Connexions of the dorsal tegmental nucleus in rat and rabbit. J. Anat. 95: 229–246, 1961.
 386. Morin, F. An experimental study of hypothalamic connections in the guinea pig. J. Comp. Neurol. 92: 193–213, 1950.
 387. Morrison, J. H., R. Benoit, P. J. Magistretti, N. Ling, and F. E. Bloom. Immunohistochemical distribution of prosomatostatin‐related peptides in hippocampus. Neurosci. Lett. 34: 137–142, 1982.
 388. Mosko, S., G. Lynch, and C. W. Cotman. The distribution of septal projections to the hippocampus of the rat. J. Comp. Neurol. 152: 163–174, 1973.
 389. Mufson, E. J., and M. M. Mesulam. Insula of the old world monkey. II. Afferent cortical input and comments on the claustrum. J. Comp. Neurol. 212: 23–27, 1982.
 390. Mufson, E. J., M. M. Mesulam, and D. N. Pandya. Insular interconnections with the amygdala in the rhesus monkey. Neuroscience 6: 1231–1248, 1981.
 391. Muhlethaler, M., J. J. Dreifuss, and B. H. Gähwiler. Vasopressin excites hippocampal neurones. Nature Lond. 296: 749–751, 1982.
 392. Murray, E. A., and M. Mishkin. Amygdalectomy impairs crossmodal association in monkeys. Science Wash. DC 228: 604–606, 1985.
 393. Nadler, J. V., C. W. Cotman, and G. S. Lynch. Subcellular distribution of transmitter‐related enzyme activities in discrete areas of the rat dentate gyrus. Brain Res. 79: 465–475, 1974.
 394. Nadler, J. V., D. A. Mathews, C. W. Cotman, and G. S. Lynch. Development of cholinergic innervation in the hippocampal formation of the rat. II. Quantitative changes in choline acetyltransferase and acetylcholinesterase activities. Dev. Biol. 36: 142–154, 1974.
 395. Nafstad, P. H. J. An electron microscope study on the termination of the perforant path fibres in the hippocampus and the fascia dentata. Z. Zellforsch. Mikrosk. Anat. 76: 532–542, 1967.
 396. Nagai, T., H. Kimura, T. Maeda, P. L. McGeer, F. Peng, and E. G. McGeer. Cholinergic projections from the basal forebrain of the rat to the amygdala. J. Neurosci. 2: 513–520, 1982.
 397. Nauta, W. J. H. Fibre degeneration following lesions of the amygdaloid complex in the monkey. J. Anat. 95: 515–532, 1961.
 398. Nauta, W. J. H. Neural associations of the amygdaloid complex in the monkey. Brain 85: 505–520, 1962.
 399. Niehoff, D. L., and M. J. Kuham. Benzodiazepine receptors: localization in rat amygdala. J. Neurosci. 3: 2091–2097, 1983.
 400. Niehoff, D. L., and P. J. Whitehouse. Multiple benzodiazepine receptors: autoradiographic localization in normal human amygdala. Brain Res. 276: 237–245, 1983.
 401. Niimi, K., M. Koizuka, S. Kawamura, and K. Abe. Efferent projections of the mamillary body in the cat. Okajimas Folia Anat. Jpn. 49: 129–156, 1972.
 402. Niimi, K., and E. Kuwahara. The dorsal thalamus of the cat and comparison with monkey and man. J. Hirnforsch. 14: 303–325, 1973.
 403. Niimi, K., H. Matsuoka, T. Aisaka, and Y. Okada. Thalamic afferents to the prefrontal cortex in the cat traced with horseradish peroxidase. J. Hirnforsch. 22: 221–241, 1981.
 404. Niimi, K., M. Niimi, and Y. Okada. Thalamic afferents to the limbic cortex in the cat studied with the method of retrograde axonal transport of horseradish peroxidase. Brain Res. 145: 225–238, 1978.
 405. Niimi, M. Cortical projections of the anterior thalamic nuclei in the cat. Exp. Brain Res. 31: 403–416, 1978.
 406. Nilges, R. G. The arteries of the mammalian cornu ammonis, J. Comp. Neurol. 80: 177–190, 1944.
 407. Nitecka, L., L. Amerski, and O. Narkiewicz. The organization of intraamygdaloid connections; an HRP study. J. Hirnforsch. 22: 3–7, 1981.
 408. Nomura, S., N. Mizuno, K. Itoh, K. Matsuda, T. Sugimoto, and Y. Nakamura. Localization of parabrachial nucleus neurons projecting to the thalamus or the amygdala in the cat using horseradish peroxidase. Exp. Neurol. 64: 375–385, 1979.
 409. Nordberg, A., C. Larsson, R. Adolfsson, and B. Winblad. Muscarinic receptor compensation in hippocampus of Alzheimer patients. J. Neural Transm. 56: 13–19, 1983.
 410. Norgren, R. Taste pathways to hypothalamus and amygdala. J. Comp. Neurol. 166: 17–30, 1976.
 411. Norita, M., and K. Kawamura. Subcortical afferents to the monkey amygdala: an HRP study. Brain Res. 190: 225–230, 1980.
 412. O'Donohue, T. L., and D. M. Jacobowitz. Studies of alpha‐MSH‐containing nerves in the brain. Prog. Biochem. Pharmacol. 16: 69–83, 1980.
 413. O'Donohue, T. L., R. L. Miller, and D. M. Jacobowitz. Identification, characterization and stereotaxic mapping of intraneuronal alpha‐melanocyte stimulating hormone‐like immunoreactive peptides in discrete regions of the rat brain. Brain Res. 176: 101–123, 1979.
 414. Ojemann, R. G. Correlations between specific human brain lesions and memory changes. Neurosci. Res. Prog. Bull. 4: 1–70, 1966.
 415. Olivier, B., R. Olivier‐Aardema, and P. R. Wiepkema. Effect of anterior hypothalamic and mammillary area lesions on the territorial aggressive behaviour in male rats. Behav. Brain Res. 9: 59–81, 1983.
 416. Olschowka, J. A., T. L. O'Donohue, G. P. Mueller, and D. M. Jacobowitz. The distribution of corticotropin releasing factor‐like immunoreactive neurons in the rat brain. Peptides Fayetteville 3: 995–1015, 1982.
 417. Olszewski, J. The Thalamus of the Macaca Mulatta. New York: Basel, 1952.
 418. Ottersen, O. P. Afferent connections to the amygdaloid complex of the rat and cat. II. Afferents from the hypothalamus and the basal telencephalon. J. Comp. Neurol. 194: 267–289, 1980.
 419. Ottersen, O. P. The afferent connections of the amygdala of the rat as studied with retrograde transport of horseradish peroxidase. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 91–104.
 420. Ottersen, O. P. Afferent connections to the amygdaloid complex of the rat with some observations in the cat. III. Afferents from the lower brain stem. J. Comp. Neurol. 202: 335–356, 1981.
 421. Ottersen, O. P. Connections of the amygdala of the rat. IV. Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J. Comp. Neurol. 205: 30–48, 1982.
 422. Ottersen, O. P., and Y. Ben‐Ari. Afferent connections to the amygaloid complex of the rat and cat. I. Projections from the thalamus. J. Comp. Neurol. 187: 401–424, 1979.
 423. Palacios, J. M., J. K. Wamsley, and M. J. Kuhar. High affinity GABA receptors—autoradiographic localization. Brain Res. 222: 285–307, 1981.
 424. Palkovits, M., L. Tapia‐Arancibia, C. Kordon, and J. Epelbaum. Somatostatin connections between the hypothalamus and the limbic system of the rat brain. Brain Res. 250: 223–228, 1982.
 425. Pandya, D. N., and H. G. J. M. Kuypers. Cortico‐cortical connections in the rhesus monkey. Brain Res. 13: 13–36, 1969.
 426. Pandya, D. N., and B. Seltzer. Association areas of the cerebral cortex. Trends Neurosci. 5: 386–390, 1982.
 427. Pandya, D. N., G. W. Van Hoesen, and V. B. Domesick. A cingulo‐amygdaloid projection in the rhesus monkey. Brain Res. 61: 369–373, 1973.
 428. Pandya, D. N., G. W. Van Hoesen, and M. M. Mesulam. Efferent connections of the cingulate gyrus in the rhesus monkey. Exp. Brain Res. 42: 319–330, 1981.
 429. Pandya, D. N., and E. H. Yeterian. Architecture and connections of cortical association areas. In: Cerebral Cortex. Association and Auditory Cortices, edited by A. Peters and E. G. Jones. New York: Plenum, 1985, vol. 4, p. 3–61.
 430. Papez, J. W. A proposed mechanism of emotion. Arch. Neurol. Psychiatry 38: 725–743, 1937.
 431. Parent, A. Distribution and morphological characteristics of acetylcholinesterase‐containing neurons in the basal forebrain of the cat. Brain Res. Bull. 8: 183–196, 1982.
 432. Pasquier, D. A., and F. Reinoso‐Suarez. Direct projections from hypothalamus to hippocampus in the rat demonstrated by retrograde transport of horseradish peroxidase. Brain Res. 108: 165–169, 1976.
 433. Pasquier, D. A., and F. Reinoso‐Suarez. Differential efferent connections of the brain stem to the hippocampus in the cat. Brain Res. 120: 540–548, 1977.
 434. Penfield, W. Functional localization in temporal and deep Sylvian areas. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 36: 210–226, 1956.
 435. Penfield, W., and H. Jasper. Epilepsy and the Functional Anatomy of the Human Brain. Boston, MA: Little, Brown, 1954.
 436. Penfield, W., and G. Mathieson. Memory autopsy findings and comments on the role of hippocampus in experiential recall. Arch. Neurol. 31: 145–154, 1974.
 437. Pearson, R. C. A., P. Brodal, K. C. Catter, and T. P. S. Powell. The organization of the connections between the cortex and the claustrum in the monkey. Brain Res. 234: 435–441, 1982.
 438. Perrett, D. I., E. T. Rolls, and W. Caan. Visual neurones responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47: 329–342, 1982.
 439. Pert, A., T. W. Moody, C. B. Pert, L. A. Dewald, and J. Rivier. Bombesin: receptor distribution in brain and effects on nociception and locomotor activity. Brain Res. 193: 209–220, 1980.
 440. Petrovicky, P. Structure and incidence of Gudden's tegmental nuclei in some mammals. Acta Anat. 80: 273–286, 1971.
 441. Ploog, D. W., and P. D. MacLean. On functions of the mamillary bodies in the squirrel monkey. Exp. Neurol. 7: 76–85, 1963.
 442. Pohle, W., T. Ott, and P. Müller‐Welde. Identification of neurons of origin providing the dopaminergic innervation of the hippocampus. J. Hirnforsch. 25: 1–10, 1984.
 443. Poletti, C. E., and G. Creswell. Fornix system efferent projections in the squirrel monkey: an experimental degeneration study. J. Comp. Neurol. 175: 101–128, 1977.
 444. Porrino, L. J., A. M. Crane, and P. S. Goldman‐Rakic. Direct and indirect pathways from the amygdala to the frontal lobe in the rhesus monkey. J. Comp. Neurol. 198: 121–136, 1981.
 445. Potter, H., and W. J. H. Nauta. A note on the problem of olfactory associations of the orbitofrontal cortex in the monkey. Neuroscience 4: 361–367, 1979.
 446. Powell, T. P. S., W. M. Cowan, and G. Raisman. The central olfactory connexions. J. Anat. 99: 791–813, 1965.
 447. Powell, T. P. S., R. W. Guillery, and W. M. Cowan. A quantitative study of the fornix‐mamillo‐thalamic system. J. Anat. 91: 419–437, 1957.
 448. Prelevic, A., W. M. Burnham, and P. Gloor. A microelectrode study of amygdaloid afferents: temporal neocortical inputs. Brain Res. 105: 437–457, 1976.
 449. Price, J. L. Toward a consistent terminology for the amygdaloid complex. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 13–18.
 450. Price, J. L. The efferent projections of the amygdaloid complex in the rat, cat and monkey. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 121–132.
 451. Price, J. L. Subeortical projections from the amygdaloid complex. In: Excitatory Amino Acids and Epilepsy, edited by Y. Ben‐Ari and R. Schwarcz. New York: Plenum, 1986, p. 19–33.
 452. Price, J. L., and D. G. Amaral. An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J. Neurosci. 1: 1242–1259, 1981.
 453. Price, J. L., and B. M. Slotnick. Dual olfactory representation in the rat thalamus: an anatomical and electrophysiological study. J. Comp. Neurol. 215: 63–77, 1983.
 454. Price, J. L., F. Russohen, and D. G. Amaral. The amygdaloid complex. In: Handbook of Chemical Neuroanatomy, edited by L. W. Swanson, A. Björklund, and T. Hökfelt. Amsterdam: Elsevier, in press.
 455. Pritzel, M., and H. J. Markowitsch. Afferents from limbic system‐related regions to the frontal cortex in the bush baby. Brain Behav. Evol. 23: 110–120, 1983.
 456. Probst, A., V. Basler, B. Bron, and J. Ulrich. Neuritic plaques in senile dementia of Alzheimer type: a Golgi analysis in the hippocampal region. Brain Res. 268: 249–254, 1983.
 457. Quirion, R., P. Gaudreau, S. St. Pierre, F. Rioux, and C. B. Pert. Autoradiographic distribution of (3H)neurotensin receptors in rat brain: visualization by tritium‐sensitive film. Peptides Fayetteville 3: 757–763, 1982.
 458. Raisman, G., W. M. Cowan, and T. P. S. Powell. The extrinsic afferent, commissural and association fibres of the hippocampus. Brain 88: 963–997, 1965.
 459. Raisman, G., W. M. Cowan, and T. P. S. Powell. An experimental analysis of the efferent projection of the hippocampus. Brain 89: 83–108, 1966.
 460. Ramón y Cajal, S. Estructura del asta de Ammon y fascia dentata. Ann. Soc. Esp. Hist. Nat. 22: 1893.
 461. Ramón y Cajal, S. Histologie du systeme nerveux de I'hommeet des vertebres. Madrid: Instituto Ramón y Cajal, 1955.
 462. Reep, R. L., and S. S. Winans. Afferent connections of dorsal and ventral agranular insular cortex in the hamster Mesocricetus auratus. Neuroscience 7: 1265–1288, 1982.
 463. Réthelyi, M., S. Vígh, G. Sétaló, I. Merchenthaler, B. Flerkó, and P. Petrusz. The luteinizing hormone releasing hormone‐containing pathways and their co‐termination with tanycyte processes in and around the median eminence and in the pituitary stalk of the rat. Acta Morphol. Acad. Sci. Hung. 29: 259–283, 1981.
 464. Ribak, C. E., and L. Seress. Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J. Neurocytol. 12: 577–597, 1983.
 465. Ribak, C. E., J. E. Vaughn, and K. Saito. Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res. 140: 315–332, 1978.
 466. Ricardo, J. A., and E. T. Koh. Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res. 153: 1–26, 1978.
 467. Riley, J. N., and R. Y. Moore. Diencephalic and brainstem afferents to the hippocampal formation of the rat. Brain Res. Bull. 6: 437–444, 1981.
 468. Roberts, G. W., Y. Allen, T. J. Crow, and J. M. Polak. Immunocytochemical localization on neuropeptides in the fornix of rat, monkey and man. Brain Res. 263: 151–155, 1983.
 469. Roberts, G. W., P. L. Woodhams, M. G. Bryant, and T. J. Crow. VIP in the rat brain: evidence for a major pathway linking the amygdala and hypothalamus via the stria terminalis. Histochemistry 65: 103–119, 1980.
 470. Roberts, G. W., P. L. Woodhams, J. M. Polak, and T. J. Crow. Distribution of neuropeptides in the limbic system of the rat: the amygdaloid complex. Neuroscience 7: 99–131, 1982.
 471. Roberts, G. W., P. L. Woodhams, J. M. Polak, and T. J. Crow. Distribution of neuropeptides in the limbic system of the rat: the hippocampus. Neuroscience 11: 35–77, 1984.
 472. Robertson, R. T., and S. S. Kaitz. Thalamic connections with limbic cortex. I. Thalamocortical projections. J. Comp. Neurol. 195: 501–525, 1981.
 473. Rodrigo Angulo, M. L. Topographical organization of the brainstem afferents to the lateral posterior‐pulvinar thalamic complex in the cat. Neuroscience 7: 1495–1508, 1982.
 474. Room, P., and H. J. Groenewegen. Connections of the parahippocampal cortex in the cat. II. Subcortical afferents. J. Comp. Neurol. 251: 451–473, 1986.
 475. Room, P., H. J. Groenewegen, and A. H. M. Lohman. Inputs from the olfactory bulb and olfactory cortex to the entorhinal cortex in the cat. Exp. Brain Res. 56: 488–496, 1984.
 476. Rose, J. Zur normalen und pathologischen Architektonik der Ammonsformation. J. Psychol. Neurol. 49: 137–192, 1938.
 477. Rose, J. The cell structure of the mamillary body in the mammals and in man. J. Anat. 74: 91–115, 1939.
 478. Rose, M. Der Allocortex bei Tier und Mensch. J. Psychol. Neurol. 34: 1–99, 1926.
 479. Rosene, D. L., and G. W. Van Hoesen. Hippocampal efferent reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science Wash. DC 198: 315–317, 1977.
 480. Ross, E. D. Disorders of recent memory in humans. Trends Neurosci. 5: 170–173, 1982.
 481. Rossor, M. N., P. C. Emson, C. Q. Mountjoy, M. Roth, and L. L. Iversen. Reduced amounts of immunoreactive somatostatin in the temporal cortex in senile dementia of Alzheimer type. Neurosci. Lett. 20: 373–377, 1980.
 482. Rossor, M. N., N. J. Garrett, A. L. Johnson, C. Q. Mountjoy, M. Roth, and L. L. Iversen. A post‐mortem study of the cholinergic and GABA systems in senile dementia. Brain 105: 313–330, 1982.
 483. Russchen, F. T. Amygdalopetal projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques. J. Comp. Neurol. 206: 159–179, 1982.
 484. Russchen, F. T. Amygdalopetal projections in the cat. II. Subcortical afferent connections. A study with retrograde tracing techniques. J. Comp. Neurol. 207: 157–176, 1982.
 485. Russchen, F. T. Cortical and subcortical afferents of the amygdaloid complex. In: Excitatory Amino Acids and Epilepsy, edited by Y. Ben‐Ari and R. Schwarcz. New York: Plenum, 1986, p. 35–52.
 486. Russchen, F. T., D. G. Amaral, and J. L. Price. The afferent connections of the substantia innominata in the monkey, Macaca fascicularis. J. Comp. Neurol. 242: 1–27, 1985.
 487. Russchen, F., D. G. Amaral, and J. L. Price. The source and thalamic termination of afferent fibers to the mediodorsal thalamic nucleus in the monkey. J. Comp. Neurol. In press.
 488. Russchen, F. T., I. Bakst, D. G. Amaral, and J. L. Price. The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res. 329: 241–257, 1985.
 489. Russchen, F. T., and J. L. Price. Amygdalostriatal projections in the rat. Topographical organizational and fiber morphology shown using the lectin PHA‐L as an anterograde tracer. Neurosci. Lett. 47: 15–22, 1984.
 490. Ruth, R. E., T. J. Collier, and R. Routtenberg. Topography between the entorhinal cortex and the dentate septotemporal axis in rats. I. Medial and intermediate entorhinal projecting cells. J. Comp. Neurol. 209: 69–78, 1982.
 491. Sagar, S. M., M. F. Beal, P. E. Marshall, D. M. Landis, and J. B. Martin. Implications of neuropeptides in neurological diseases. Peptides Fayetteville 5: 255–262, 1984.
 492. Sakumoto, T., K. Sakai, M. Jouvet, H. Kimura, and T. Maeda. 5‐HT immunoreactive hypothalamic neurons in rat and cat after 5‐HTP administration. Brain Res. Bull. 12: 721–733, 1984.
 493. Saper, C. B. Convergence of autonomic and limbic connections in the insular cortex of the rat. J. Comp. Neurol. 210: 163–173, 1982.
 494. Saper, C. B., and A. D. Loewy. Efferent connections of the parabrachial nucleus in the rat. Brain Res. 197: 291–317, 1980.
 495. Saper, C. B., L. W. Swanson, and W. M. Cowan. The efferent connections of the ventromedial nucleus of the hypothalamus of the rat. J. Comp. Neurol. 169: 409–442, 1976.
 496. Saper, C. B., L. W. Swanson, and W. M. Cowan. The efferent connections of the anterior hypothalamic area of the rat, cat and monkey. J. Comp. Neurol. 182: 575–599, 1978.
 497. Sar, M., W. E. Stumpf, R. J. Miller, K. J. Chang, and P. Cuatrecasas. Immunohistochemical localization of enkephalin in rat brain and spinal cord. J. Comp. Neurol. 182: 17–37, 1978.
 498. Sarter, M., and H. J. Markowitsch. Convergence of basolateral amygdaloid and mediodorsal thalamic projections in different areas of the frontal cortex in the rat. Brain Res. Bull. 10: 607–622, 1983.
 499. Sarter, M., and H. J. Markowitsch. Collateral innervation of the medial and lateral prefrontal cortex by amygdaloid, thalamic, and brain‐stem neurons. J. Comp. Neurol. 224: 445–460, 1984.
 500. Sarter, M., and H. J. Markowitsch. The amygdala's role in human mnemonic processing. Cortex 21: 7–24, 1985.
 501. Sarter, M., and H. J. Markowitsch. Involvement of the amygdala in learning and memory: a critical review, with emphasis on anatomical relations. Behav. Neurosci. 99: 342–380, 1985.
 502. Sata, M., K. Itoh, and N. Mizuno. Distribution of thalamocaudate neurons in the cat as demonstrated by horseradish peroxidase. Exp. Brain Res. 34: 143–153, 1979.
 503. Scalia, F., and S. S. Winans. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161: 31–56, 1975.
 504. Scheibel, A. B. The hippocampus: organizational patterns in health and senescence. Mech. Ageing Dev. 9: 89–102, 1979.
 505. Scheibel, A. B. Dendritic changes. In: Alzheimer's Disease, edited by B. Reisberg. New York: Free Press, 1983, p. 69–73.
 506. Schmechel, D. E., B. G. Vickrey, D. Fitzpatrick, and R. P. Elde. GABAergic neurons of mammalian cerebral cortex: widespread subclass defined by somatostatin content. Neurosci. Lett. 47: 227–232, 1984.
 507. Schwaber, J. S., B. S. Kapp, G. A. Higgins, and P. R. Rapp. Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J. Neurosci. 2: 1424–1438, 1982.
 508. Schwartzkroin, P. A., and D. D. Kunkel. Morphology of identified interneurons in the CAl regions of guinea pig hippocampus. J. Comp. Neurol. 232: 205–218, 1985.
 509. Scoville, W. B., and B. Milner. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20: 11–21, 1957.
 510. Segal, M. Brain stem afferents to the rat medial septum. J. Physiol. Lond. 261: 617–631, 1976.
 511. Segal, M. Afferents to the entorhinal cortex of the rat studied by the method of retrograde transport of horseradish peroxidase. Exp. Neurol. 57: 750–765, 1977.
 512. Segal, M. A potent inhibitory monosynaptic hypothalamo‐hippocampal connection. Brain Res. 162: 137–141, 1979.
 513. Segal, M., and F. E. Bloom. The action of norepinephrine in the rat hippocampus. II. Activation of the input pathway. Brain Res. 72: 99–114, 1974.
 514. Segal, M., and S. Landis. Afferents to the hippocampus of the rat studied with the method of retrograde transport of horseradish peroxidase. Brain Res. 78: 1–15, 1974.
 515. Seki, M., and K. Zyo. Anterior thalamic afferents from the mamillary body and the limbic cortex in the rat. J. Comp. Neurol. 229: 242–256, 1984.
 516. Seltzer, B., and D. N. Pandya. Some cortical projections to the parahippocampal area in the rhesus monkey. Exp. Neurol. 50: 146–160, 1976.
 517. Seltzer, B., and D. N. Pandya. Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res. 149: 1–24, 1978.
 518. Seltzer, B., and D. N. Pandya. Further observations on parieto‐temporal connections in the rhesus monkey. Exp. Brain Res. 55: 301–312, 1984.
 519. Seltzer, B., and G. W. Van Hoesen. A direct inferior parietal lobule projection to the presubiculum in the rhesus monkey. Brain Res. 179: 157–161, 1979.
 520. Seress, L. Pyramid‐like basket cells in the granular layer of the dentate gyrus in the rat. J. Anat. 127: 163–168, 1978.
 521. Seress, L., and J. Pokorny. Structure of the granular layer of the rat dentate gyrus. A light microscope and Golgi study. J. Anat. 133: 181–195, 1981.
 522. Seress, L., and C. E. Ribak. GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp. Brain Res. 50: 173–182, 1983.
 523. Sethy, V. H., R. H. Roth, M. J. Kuhar, and M. H. Van Woert. Choline and acetylcholine: regional distribution and effects of degeneration of cholinergic nerve terminals in the rat hippocampus. Neuropharmacology 12: 819–823, 1973.
 524. Sgonina, K. Zur vergleichenden Anatomie der entorhinal—und Prasubikularregion. J. Psychol. Neurol. 48: 56–163, 1938.
 525. Shefer, V. F. Hippocampal pathology as a possible factor in the pathogenesis of senile dementias. Neurosci. Behav. Physiol. 8: 236–239, 1977.
 526. Shen, C. L. Efferent projections from the mamillary complex of the guinea pig: an autoradiographic study. Brain Res. Bull. 11: 43–59, 1983.
 527. Sherlock, D. A., and G. Raisman. A comparison of anterograde and retrograde axonal transport of horseradish peroxidase in the connections of the mammillary nuclei in the rat. Brain Res. 85: 321–324, 1975.
 528. Shipley, M. T. Presubiculum afferents to the entorhinal area and the Papez circuit. Brain Res. 67: 162–168, 1974.
 529. Shipley, M. T. The topographical and laminar organization of the presubiculum's projection to the ipsi‐ and contralateral entorhinal cortex in the guinea pig. J. Comp. Neurol. 160: 127–146, 1975.
 530. Shipley, M. T., and K. E. Sorensen. On the laminar organization of the anterior thalamus projections to the presubiculum in the guinea pig. Brain Res. 86: 473–477, 1975.
 531. Shults, C. W., R. Quirion, B. Chronwall, T. N. Chase, and T. L. O'Donohue. A comparison of the anatomical distribution of substance P and substance P receptors in the rat central nervous system. Peptides Fayetteville 5: 1097–1128, 1984.
 532. Siegel, A., H. Edinger, and S. Ohgami. The topographical organization of the hippocampal projection to the septal area: a comparative neuroanatomical analysis in the gerbil, rat, rabbit, and cat. J. Comp. Neurol. 157: 359–378, 1974.
 533. Siegel, A., S. Ohgami, and H. Edinger. Projections of the hippocampus to the septal area in the squirrel monkey. Brain Res. 99: 247–260, 1975.
 534. Siggins, G. R., J. F. McGinty, J. H. Morrison, Q. J. Pittman, W. Zieglgänsberger, P. J. Magistretti, and D. L. Gruol. Role of neuropeptides in the hippocampal formation. In: Advances in Biochemical Psychopharmacology. Regulatory Peptides From Molecular Biology to Function, edited by G. Costa and M. Trabucchi. New York: Raven, 1982, vol. 33, p. 413–422.
 535. Silverman, A. J., J. L. Antunes, G. M. Abrams, G. Nilaver, R. Thau, J. A. Robinson, M. Ferin, and L. C. Krey. The luteinizing hormone‐releasing hormone pathways in rhesus and pigtailed monkeys: new observations on thick, unembedded sections. J. Comp. Neurol. 211: 309–317, 1982.
 536. Silverman, A. J., and L. C. Krey. The luteinizing hormone‐releasing hormone (LH‐RH) neuronal networks of the guinea pig brain. I. Intra‐ and extra‐hypothalamic projections. Brain Res. 157: 233–246, 1978.
 537. Simantov, R., M. J. Kuhar, G. W. Pasternak, and S. H. Snyder. The regional distribution of a morphine‐like factor enkephalin in monkey brain. Brain Res. 106: 189–197, 1976.
 538. Simmons, R. M. The morphology of the diencephalon in the Prosimii. II. The Lemuroidea and Lorisoidea. Pt. II. Epithalamus, subthalamus and hypothalamus. J. Hirnforsch. 21: 493–514, 1980.
 539. Simpson, D. A. The efferent fibres of the hippocampus in the monkey. J. Neurol. Neurosurg. Psychiatry 15: 79–92, 1952.
 540. Sims, K. B., D. L. Hoffman, S. I. Said, and E. A. Zimmerman. Vasoactive intestinal polypeptide (VIP) in mouse and rat brain: an immunocytochemical study. Brain Res. 186: 165–183, 1980.
 541. Sloniewski, P., K. G. Usunoff, and C. H. Pilgrim. Retrograde transport of fluorescent tracers reveals extensive ipsi‐and contralateral claustrocortical connections in the rat. J. Comp. Neurol. 246: 467–477, 1986.
 542. Smialowski, A. Amygdaloid complex of the macaque. Acta Biol. Exp. 25: 77–89, 1965.
 543. Smith, Y., A. Parent, L. Kerkerian, and G. Pelletier. Distribution of neuropeptide Y immunoreactivity in the basal forebrain and upper brainstem of the squirrel monkey (Saimiri sciureus). J. Comp. Neurol. 236: 71–89, 1985.
 544. Sofroniew, M. V. Morphology of vasopressin and oxytocin neurones and their central and vascular projections. In: Progress in Brain Research. The Neurohypophysis: Structure, Function and Control, edited by B. A. Cross and G. Leng. Amsterdam: Elsevier, 1983, vol. 60, p. 101–114.
 545. Sofroniew, M. V. Vasopressin‐ and neurophysin‐immuno‐reactive neurons in the septal region, medial amygdala and locus coeruleus in colchicine‐treated rats. Neuroscience 15: 347–358, 1985.
 546. Sofroniew, M. V., A. Weindl, U. Schrell, and R. Wetzstein. Immunohistochemistry of vasopressin, oxytocin and neurophysin in the hypothalamus and extrahypothalamic regions of the human and primate brain. Acta Histochem. 24: 79–95, 1981.
 547. Sommer, W. Erkrankung des Ammonshorns als Aetiologisches moment der Epilepsie. Arch. Psychiatr. Nervenkr. 10: 631–675, 1880.
 548. Somogyi, P., M. G. Nunzi, A. Gorio, and A. D. Smith. A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res. 259: 137–142, 1983.
 549. Sørensen, K. E. Projections of the entorhinal area to the striatum, nucleus accumbens, and cerebral cortex in the guinea pig. J. Comp. Neurol. 238: 308–322, 1985.
 550. Sørensen, K. E., and M. T. Shipley. Projections from the subiculum to the deep layers of the ipsilateral presubicular and entorhinal cortices in the guinea pig. J. Comp. Neurol. 188: 313–334, 1979.
 551. Sørensen, K. E., and M. P. Witter. Entorhinal efferents reach the caudato‐putamen. Neurosci. Lett. 35: 259–264, 1983.
 552. Squire, L. R. The neuropsychology of human memory. Annu. Rev. Neurosci. 5: 241–273, 1982.
 553. Squire, L. R., N. J. Cohen, and L. Nadel. The medial temporal region and memory consolidation: a new hypothesis. In: Memory Consolidation, edited by H. Weingartner and E. Parker. Hillsdale, NJ: Erlbaum, 1984, p. 185–210.
 554. Squire, L. R., and R. Y. Moore. Dorsal thalamic lesion in a noted case of human memory dysfunction. Ann. Neurol. 6: 503–506, 1979.
 555. Squire, L. R., and S. Zola‐Morgan. The neurology of memory: the case for correspondence between the findings for human and nonhuman primate. In: The Physiological Basis of Memory (2nd ed.), edited by J. A. Deutsch. New York: Academic, 1983, p. 199–268.
 556. Sripanidkulchai, K., B. Sripanidkulchai, and J. M. Wyss. The cortical projection of the basolateral amygdaloid nucleus in the rat: a retrograde fluorescent dye study. J. Comp. Neurol. 229: 419–431, 1984.
 557. Stengaard‐Pedersen, K. Inhibition of enkephalin binding to opiate receptors by zinc ions: possible physiological importance in the brain. Acta Pharmacol. 50: 213–220, 1982.
 558. Stengaard‐Pedersen, K. Comparative mapping of opioid receptors and enkephalin immunoreactive nerve terminals in the rat hippocampus. Histochemistry 79: 311–333, 1983.
 559. Stengaard‐Pedersen, K., K. Fredens, and L. I. Larsson. Comparative localization of enkephalin and cholecystokinin immunoreactivities and heavy metals in the hippocampus. Brain Res. 273: 81–96, 1983.
 560. Stephan, H. Handbuch der Mikroskopischen Anatomie des Menschen: Allocortex. Berlin: Springer‐Verlag, 1975.
 561. Stephan, H. Evolutionary trends in limbic structures. Neurosci. Behav. Rev. 7: 367–374, 1983.
 562. Stephan, H. and O. J. Andy. The allocortex in primates. In: The Primate Brain, edited by C. R. Noback and W. Montagna. New York: Appleton‐Century‐Crofts, 1970, p. 109–135.
 563. Stephan, H., and J. Manolescu. Comparative investigation on hippocampus in insectivores and primates. Z. Mikrosk. Anat. Forsch. Leipz. 94: 1025–1050, 1980.
 564. Steward, O. Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. Comp. Neurol. 167: 285–314, 1976.
 565. Steward, O., and S. A. Scoville. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169: 347–370, 1976.
 566. Storm‐Mathisen, J. Quantitative histochemistry of acetylcholinesterase in rat hippocampal region correlated to histo‐chemical staining. J. Neurochem. 17: 739–750, 1970.
 567. Storm‐Mathisen, J. Localization of putative transmitters in the hippocampal formation. Ciba Found. Symp. 58: 49–86, 1977.
 568. Storm‐Mathisen, J. Glutamate in hippocampal pathways. In: Glutamate as a Neurotransmitter, edited by G. Di Chiara and G. L. Gessa. New York: Raven, 1981, p. 43–55.
 569. Storm‐Mathisen, J., and T. W. Blackstad. Cholinesterase in the hippocampal region. Acta Anat. 56: 216–253, 1964.
 570. Storm‐Mathisen, J., and F. Fonnum. Localization of transmitter candidates in the hippocampal region. In: Progress in Brain Research. Biochemical and Pharmacological Mechanisms Underlying Behaviour, edited by P. B. Bradley and R. W. Brimblecombe. Amsterdam: Elsevier, 1972, vol. 36, p. 41–58.
 571. Storm‐Mathisen, J., A. K. Leknes, A. T. Bore, J. L. Vaaland, P. Edminson, F. M. S. Haug, and O. P. Ottersen. First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature Lond. 301: 517–520, 1983.
 572. Storm‐Mathisen, J., and M. W. Opsahl. Asparate and/or glutamate may be transmitters in hippocampal efferents to septum and hypothalamus. Neurosci. Lett. 9: 65–70, 1978.
 573. Struble, R. G., N. L. Desmond, and W. B. Levy. Anatomical evidence for interlamellar inhibition in the fascia dentata. Brain Res. 152: 580–585, 1978.
 574. Swanson, L. W. An autoradiographic study of the efferent connections of the preoptic region in the rat. J. Comp. Neurol. 167: 227–256, 1976.
 575. Swanson, L. W. The anatomical organization of septo‐hippocampal projections. In: Functions of the Septo‐Hippocampal System. Amsterdam: Elsevier/North‐Holland, 1978, p. 25–48. (Ciba Found. Symp. 58).
 576. Swanson, L. W. The hippocampus—new anatomical insights. Trends Neurosci. 2: 9–12, 1979.
 577. Swanson, L. W. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res. 217: 150–154, 1981.
 578. Swanson, L. W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9: 321–353, 1982.
 579. Swanson, L. W. The hippocampus and the concept of the limbic system. In: Neurobiology of the Hippocampus, edited by W. Seifert. New York: Academic, 1983, p. 3–19.
 580. Swanson, L. W., and W. M. Cowan. Hippocampo‐hypothalamic connections: origin in subicular cortex, not Ammon's horn. Science Wash. DC 189: 303–304, 1975.
 581. Swanson, L. W., and W. M. Cowan. Autoradiographic studies of the development and connections of the septal area in the rat. In: The Septal Nuclei, edited by J. W. DeFrance. New York: Plenum, 1976, p. 37–64.
 582. Swanson, L. W., and W. M. Cowan. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 172: 49–84, 1977.
 583. Swanson, L. W., and W. M. Cowan. The connections of the septal region in the rat. J. Comp. Neurol. 186: 621–655, 1979.
 584. Swanson, L. W., and B. K. Hartman. The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamines‐β‐hydroxylase as a marker. J. Comp. Neurol. 163: 467–506, 1975.
 585. Swanson, L. W., and C. Köhler. Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J. Neurosci. 6: 3010–3023, 1986.
 586. Swanson, L. W., P. E. Sawchenko, and W. M. Cowan. Evidence that the commissural, associational and septal projections of the regio inferior of the hippocampus arise from the same neurons. Brain Res. 197: 207–212, 1980.
 587. Swanson, L. W., P. E. Sawchenko, and W. M. Cowan. Evidence for collateral projections by neurons in Ammon's horn, the dentate gyrus, and the subiculum: a multiple retrograde labeling study in the rat. J. Neurosci. 1: 548–559, 1981.
 588. Swanson, L. W., P. E. Sawchenko, J. Rivier, and W. W. Vale. Organization of ovine corticotropin‐releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36: 165–186, 1983.
 589. Swanson, L. W., J. M. Wyss, and W. M. Cowan. An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J. Comp. Neurol. 181: 681–716, 1978.
 590. Takagi, S. F. The olfactory nervous system of the old world monkey. Jpn. J. Physiol. 34: 561–573, 1984.
 591. Takeuchi, Y., S. Matsushima, R. Matsushima, and D. A. Hopkins. Direct amygdaloid projections to the dorsal motor nucleus of the vagus nerve: a light and electron microscopic study in the rat. Brain Res. 280: 143–147, 1983.
 592. Takeuchi, Y., J. H. McLean, and D. A. Hopkins. Reciprocal connections between the amygdala and parabrachial nuclei: ultrastructural demonstration by degeneration and axonal transport of horseradish peroxidase in the cat. Brain Res. 239: 583–588, 1982.
 593. Tanaka, D. Thalamic projections of the dorsomedial prefrontal cortex in the rhesus monkey (Macaca mulatta). Brain Res. 110: 21–38, 1976.
 594. Taxt, T., and J. Storm‐Mathisen. Uptake of d‐aspartate and l‐glutamate in excitatory axon terminals in hippocampus: autoradiographic and biochemical comparison with y‐amino‐butyrate and other amino acids in normal rats and in rats with lesions. Neuroscience 11: 79–100, 1984.
 595. Terry, R. D., and R. Katzman. Senile dementia of the Alzheimer type. Ann. Neurol. 14: 497–506, 1983.
 596. Tielen, A. M., F. W. Van Leeuwen, and F. H. Lopes DA Silva. The localization of leucine‐enkephalin immunoreactivity within the guinea pig hippocampus. Exp. Brain Res. 48: 288–295, 1982.
 597. Tigges, J., M. Tigges, N. A. Cross, R. L. McBride, W. D. Letbetter, and S. Anschel. Subcortical structures projecting to visual cortical areas in squirrel monkey. J. Comp. Neurol. 209: 29–40, 1982.
 598. Tigges, J., L. C. Walker, and M. Tigges. Subcortical projections to the occipital and parietal lobes of the chimpanzee brain. J. Comp. Neurol. 220: 106–115, 1983.
 599. Tobias, T. J. Afferents to prefrontal cortex from the thalamic mediodorsal nucleus in the rhesus monkey. Brain Res. 83: 191–212, 1975.
 600. Tömböl, T. Cellular and synaptic organization of the dorsomedial thalamic nucleus. Acta Morphol. Acad. Sci. Hung. 16: 183–203, 1968.
 601. Tömböl, T., M. Babosa, and P. Somogyi. Interneurons: an electron microscopic study of the cat's hippocampal formation. II. Acta Morphol. Acad. Sci. Hung. 27: 297–313, 1979.
 602. Triepel, J., and C. J. Grimmelikhuijzen. Mapping of neurons in the central nervous system of the guinea pig by use of antisera specific to the molluscan neuropeptide FMRFamide. Cell Tissue Res. 237: 575–586, 1984.
 603. Trojanowski, J. Q., and S. Jacobson. Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey. J. Comp. Neurol. 169: 371–392, 1976.
 604. Turner, B. H., K. C. Gupta, and M. Mishkin. The locus and cytoarchitecture of the projection areas of the olfactory bulb in Macaca mulatta. J. Comp. Neurol. 177: 381–396, 1978.
 605. Turner, B. H., and M. E. Knapp. Projections of the nucleus and tracts of the stria terminalis following lesions at the level of the anterior commissure. Exp. Neurol. 51: 468–479, 1976.
 606. Turner, B. H., M. Mishkin, and M. E. Knapp. Distribution of the anterior commissure to the amygdaloid complex in the monkey. Brain Res. 162: 331–337, 1979.
 607. Turner, B. H., M. Mishkin, and M. Knapp. Organization of the amygdalopetal projections from modality‐specific cortical association areas in the monkey. J. Comp. Neurol. 191: 515–543, 1980.
 608. Turner, B. H., and J. Zimmer. The architecture and some of the interconnections of the rat's amygdala and lateral periallocortex. J. Comp. Neurol. 227: 540–557, 1984.
 609. Uchida, Y. A contribution to the comparative anatomy of the amygdaloid nuclei in mammals, especially in rodents. Part I: rat and mouse. Folia Psychiatr. Neurol. Jpn. 4: 25–42, 1950.
 610. Uchida, Y. A contribution to the comparative anatomy of the amygdaloid nuclei in mammals, especially in rodents. Part II: guinea pig, rabbit and squirrel. Folia Psychiatr. Neurol. Jpn. 4: 91–107, 1950.
 611. Uhl, G. R., R. R. Goodman, M. J. Kuhar, S. R. Childers, and S. H. Snyder. Immunohistochemical mapping of enkephalin containing cell bodies, fibers and nerve terminals in the brain stem of the rat. Brain Res. 166: 75–94, 1979.
 612. Uhl, G. R., R. R. Goodman, M. J. Kuhar, and S. H. Snyder. Enkephalin and neurotensin: immunohistochemical localization and identification of an amygdalofugal pathway. Adv. Biochem. Psychopharmacol. 18: 71–87, 1978.
 613. Ulrich, J. Alzheimer changes in nondemented patients younger than sixty‐five: possible early stages of Alzheimer's disease and senile dementia of Alzheimer type. Ann. Neurol. 17: 273–277, 1985.
 614. Ulrich, J., and H. B. Stähelin. The variable topography of Alzheimer type changes in senile dementia and normal old age. Gerontology 30: 210–214, 1984.
 615. Van der Kooy, D., and L. Y. Koda. Organization of the projections of a circumventricular organ: the area postrema in the rat. J. Comp. Neurol. 219: 328–338, 1983.
 616. Van der Kooy, D., H. G. J. M. Kuypers, and C. E. Catsman‐Berrevoets. Single mammillary body cells with divergent axon collaterals. Demonstration by a simple, fluorescent retrograde double labeling technique in the rat. Brain Res. 158: 189–196, 1978.
 617. Van Essen, D. C., and J. H. R. Maunsell. Hierarchical organization and functional streams in the visual cortex. Trends Neurosci. 6: 370–374, 1983.
 618. Van Hoesen, G. W. The differential distribution, diversity and sprouting of cortical projections to the amygdala in the rhesus monkey. In: The Amygdaloid Complex, edited by Y. Ben‐Ari. Amsterdam: Elsevier/North‐Holland, 1981, p. 77–90.
 619. Van Hoesen, G. W. The parahippocampal gyrus. New observations regarding its cortical connections in the monkey. Trends Neurosci. 5: 345–350, 1982.
 620. Van Hoesen, G. W., and D. N. Pandya. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res. 95: 1–24, 1975.
 621. Van Hoesen, G. W., and D. N. Pandya. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res. 95: 39–59, 1975.
 622. Van Hoesen, G. W., D. N. Pandya, and N. Butters. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents. Brain Res. 95: 25–38, 1975.
 623. Van Hoesen, G. W., D. L. Rosene, and M. M. Mesulam. Subicular input from temporal cortex in the rhesus monkey. Science Wash. DC 205: 608–610, 1979.
 624. Van Hoesen, G. W., E. H. Yeterian, and R. Lavizzo‐Mourey. Widespread corticostriate projections from temporal cortex of the rhesus monkey. J. Comp. Neurol. 199: 205–219, 1981.
 625. Van Wimersma Greidanus, T. B., B. Bohus, G. L. Kovacs, D. H. Versteeg, J. P. Bubach, and D. De Wied. Sites of behavioral and neurochemical action of ACTH‐like peptides and neurohypophyseal hormones. Neurosci. Biobehav. Rev. 7: 453–463, 1983.
 626. Veazey, R. B., D. G. Amaral, and W. M. Cowan. The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). I. Cytoarchitectonic organization. J. Comp. Neurol. 207: 114–134, 1982.
 627. Veazey, R. B., D. G. Amaral, and W. M. Cowan. The morphology and connections of the posterior hypothalamus in the cynomolgus monkey. II. Efferent connections. J. Comp. Neurol. 207: 135–156, 1982.
 628. Veazey, R. B., and C. M. Severin. Efferent projections of the deep mesencephalic nucleus (pars lateralis) in the rat. J. Comp. Neurol. 190: 231–244, 1980.
 629. Veening, J. G. Cortical afferents of the amygdaloid complex in the rat: an HRP study. Neurosci. Lett. 8: 191–195, 1978.
 630. Veening, J. G. Subcortical afferents of the amygdaloid complex in the rat: an HRP study. Neurosci. Lett. 8: 197–202, 1978.
 631. Veening, J. G., L. W. Swanson, and P. E. Sawchenko. The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport‐immunohisto‐chemical study. Brain Res. 303: 337–357, 1984.
 632. Velayos, J. L., and F. Reinoso‐Suarez. Topographic organization of the brainstem afferents to the mediodorsal thalamic nucleus. J. Comp. Neurol. 206: 17–27, 1982.
 633. Verney, C., M. Baulac, B. Berger, C. Alvarez, A. Vigny, and K. B. Helle. Morphological evidence for a dopaminergic terminal field in the hippocampal formation of young and adult rat. Neuroscience 14: 1039–1052, 1985.
 634. Victor, M., R. D. Adams, and G. H. Collins. The Wernicke‐Korsakoff Syndrome. Philadelphia, PA: Davis, 1971.
 635. Vilkki, J. Effects of thalamic lesions on complex perception and memory. Neuropsychologia 16: 427–437, 1978.
 636. Vincent, S. R., T. Hökfelt, L. R. Skirboll, and J. Y. Wu. Hypothalamic γ‐aminobutyric acid neurons project to the neocortex. Science Wash. DC 220: 1309–1311, 1983.
 637. Vincent, S. R., H. Kimura, and E. G. McGeer. Organization of substance P fibers within the hippocampal formation demonstrated with a biotin‐avidin immunoperoxidase technique. J. Comp. Neurol. 199: 113–123, 1981.
 638. Vincent, S. R., and E. G. McGeer. A substance P projection to the hippocampus. Brain Res. 215: 349–351, 1981.
 639. Vogt, B. A. Cingulate cortex. In: Cerebral Cortex. Association and Auditory Cortices, edited by A. Peters and E. G. Jones. New York: Plenum, vol. 4, 1985, p. 89–149.
 640. Vogt, B. A., D. L. Rosene, and D. N. Pandya. Thalamic and cortical afferents differentiate anterior from posterior cingulate cortex in the monkey. Science Wash. DC 204: 205–207, 1979.
 641. Volsch, M. Zur vergleichenden Anatomie des Mandelkernes und seine Nachbargebilde. Part I. Arch. Mikrosk. Anat. 68: 573–683, 1906.
 642. volsch, M. Zur vergleichenden Anatomie des Mandelkernes und seine Nachbargebilde. Part II. Arch. Mikrosk. Anat. 76: 373–523, 1910.
 643. Wainer, B. H., A. I. Levey, D. B. Rye, and M. M. Mesulam. Cholinergic and non‐cholinergic septohippocampal pathways. Neurosci. Lett. 54: 45–52, 1985.
 644. Wakefield, C. The intrinsic connections of the basolateral amygdaloid nuclei as visualized with the HRP method. Neurosci. Lett. 12: 17–21, 1979.
 645. Wakefield, C., and E. Hall. Some observations on the ultrastructure of the central amygdaloid nucleus in the cat. Cell Tissue Res. 151: 489–498, 1974.
 646. Wakefield, C., and E. Hall. Hypothalamic projections to the amygdala in the cat. Cell Tissue Res. 151: 499–508, 1974.
 647. Walker, A. E. A cytoarchitectural study of the prefrontal area of the macaque monkey. J. Comp. Neurol. 73: 59–86, 1940.
 648. Walker, J. E., and F. Fonnum. Regional cortical glutamergic and aspartergic projections to the amygdala and thalamus of the rat. Brain Res. 267: 371–374, 1983.
 649. Wansley, J. K., W. S. Young, and M. J. kuhar. Immunohistochemical localization of enkephalin in rat forebrain. Brain Res. 190: 153–174, 1980.
 650. Warrington, E. K., and L. Weiskrantz. Amnesia: a disconnection syndrome? Neuropsychologia 20: 233–248, 1982.
 651. Watanabe, K., and E. Kawana. A horseradish peroxidase study on the mammillothalamic tract in the rat. Acta Anat. 108: 394–401, 1980.
 652. Watson, S. J., C. W. Richard, and J. D. Barchas. Adrenocorticotropin in rat brain: immunocytochemical localization in cells and axons. Science Wash. DC 200: 1180–1182, 1978.
 653. Weindl, A., and M. V. Sofroniew. Demonstration of extra‐hypothalamic peptide secreting neurons. A morphologic contribution to the investigation of psychotropic effects of neurohormones. Pharmakopsychiatr. Neuropsychopharmakol. 9: 226–234, 1976.
 654. Weiskrantz, L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol. 49: 381–391, 1956.
 655. Weiskrantz, L. Comparative aspects of studies of amnesia. Philos. Trans. R. Soc. Lond. B Biol Sci. 298: 97–109, 1982.
 656. Werling, L. L., and J. V. Nadler. Evidence for differential localization of two binding sites for l‐[3H]glutamate in rat fascia dentata. Brain Res. 276: 344–347, 1983.
 657. West, C. H. K., J. C. Jackson, and R. M. Benjamin. An autoradiographic study of subcortical forebrain projections from mediodorsal and adjacent midline thalamic nuclei in the rabbit. Neuroscience 4: 1977–1988, 1979.
 658. West, J. R., H. O. Nornes, C. L. Barnes, and M. Bronfenbrenner. The cells of origin of the commissural afferents to the area dentata in the mouse. Brain Res. 160: 203–216, 1979.
 659. White, W. F., J. V. Nadler, A. Hamberger, C. W. Cotman, and J. T. Cummins. Glutamate as transmitter of hippocampal perforant path. Nature Lond. 270: 356–357, 1977.
 660. Whiteley, A. M., and E. K. Warrington. Prosopagnosia: a clinical, psychological, and anatomical study of three patients. J. Neurol. Neurosurg. Psychiatry 40: 395–403, 1977.
 661. Whitlock, D. G., and W. J. H. Nauta. Subcortical projections from the temporal neocortex in macaca mulatta. J. Comp. Neurol. 106: 183–212, 1956.
 662. Wickelgren, W. A. Chunking and consolidation: a theoretical synthesis of semantic networks, configuring in conditioning, S‐R versus cognitive learning, normal forgetting, the amnesic syndrome, and the hippocampal arousal system. Psychol. Rev. 86: 44–60, 1979.
 663. Wieraszko, A. Glutamic and aspartic acid as putative neurotransmitters: release and uptake studies on hippocampal slices. In: Neurobiology of the Hippocampus, edited by W. Seifert. New York: Academic, 1983, p. 175–196.
 664. Wilhite, B. L., T. J. Teyler, and C. Hendricks. Functional relations of the rodent claustral‐entorhinal‐hippocampal system. Brain Res. 365: 54–60, 1986.
 665. Wilkinson, A., and I. Davies. The influence of age and dementia on the neuron population of the mamillary bodies. Age Ageing 7: 151–160, 1978.
 666. Williams, R. G., and G. J. Dockray. Distribution of enkephalin‐related peptides in rat brain: immunohistochemical studies using antisera to met‐enkephalin and met‐enkephalin Arg6Phe7. Neuroscience 9: 563–586, 1983.
 667. Witt, E. D., and P. S. Goldman‐Rakic. Intermittent thiamine deficiency in the rhesus monkey. I. Progression of neurological signs and neuroanatomical lesions. Ann. Neurol. 13: 376–394, 1983.
 668. Witt, E. D., and P. S. Goldman‐Rakic. Intermittent thiamine deficiency in the rhesus monkey. II. Evidence for memory loss. Ann. Neurol. 13: 396–401, 1983.
 669. Witter, M. P., and H. J. Groenewegen. Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat. J. Comp. Neurol. 224: 371–385, 1984.
 670. Witter, M. P., H. J. Groenewegen, and F. T. Russchen. Entorhinal and perirhinal projections to the striatum, amygdala and claustrum in the cat; a neuroanatomical study using anterograde and retrograde transport techniques. Neurosci. Lett. Suppl. 7: 544, 1981.
 671. Woolf, N. J., and L. L. Butcher. Cholinergic projections to the basolateral amygdala: a combined Evans blue and acetylcholinesterase analysis. Brain Res. Bull. 8: 751–763, 1982.
 672. Wray, S., and G. E. Hoffman. Organization and interrelationship of neuropeptides in the central amygdaloid nucleus of the rat. Peptides Fayetteville 4: 525–541, 1983.
 673. Wyss, J. M., L. W. Swanson, and W. M. Cowan. Evidence for an input to the molecular layer and the stratum granulosum of the dentate gyrus from the supramammillary region of the hypothalamus. Anat. Embryol. 156: 165–176, 1979.
 674. Wyss, J. M., L. W. Swanson, and W. M. Cowan. A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4: 463–476, 1979.
 675. Yarita, H., M. Iino, T. Tanabe, S. Kogure, and S. F. Takagi. A transthalamic olfactory pathway to orbitofrontal cortex in the monkey. J. Neurophysiol. 43: 69–85, 1980.
 676. Young, W. S., G. F. Alheid, and L. Heimer. The ventral pallidal projection to the mediodorsal thalamus: a study with fluorescent retrograde tracers and immunohistofluorescence. J. Neurosci. 4: 1626–1638, 1984.
 677. Young, W. S., and M. J. Kuhar. Neurotensin receptor localization by light microscopic autoradiography in rat brain. Brain Res. 206: 273–285, 1981.
 678. Záborszky, L., C. S. Léránth, and L. Heimer. Ultrastructural evidence of amygdalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci. Lett. 52: 219–225, 1984.
 679. Zarbin, M. A., R. B. Innis, J. K. Wamsley, S. H. Snyder, and M. J. Kuhar. Autoradiographic localization of cholecystokinin receptors in rodent brain. J. Neurosci. 3: 877–906, 1983.
 680. Zimmer, J. Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation. J. Comp. Neurol. 142: 393–416, 1971.
 681. Zimmer, J. Extended commissural and ipsilateral projections in post‐natally deentorhinated hippocampus and fascia dentata demonstrated in rats by silver impregnation. Brain Res. 64: 293–311, 1973.
 682. Zola‐Morgan, S., and L. Squire. Amnesia in monkeys after lesions of the mediodorsal nucleus of the thalamus. Ann. Neurol. 17: 558–564, 1985.
 683. Zola‐Morgan, S., L. Squire, and D. G. Amaral. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CAl of the hippocampus. J. Neurosci. 6: 2950–2967, 1986.
 684. Zola‐Morgan, S., L. R. Squire, and M. Mishkin. The neuroanatomy of amnesia: amygdala‐hippocampus versus temporal stem. Science Wash. DC 218: 1337–1339, 1982.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

David G. Amaral. Memory: Anatomical Organization of Candidate Brain Regions. Compr Physiol 2011, Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain: 211-294. First published in print 1987. doi: 10.1002/cphy.cp010507