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Central Neural Mechanisms of Hearing

L. M. Aitkin, D. R. F. Irvine, W. R. Webster

10.1002/cphy.cp010316

Source: Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes

Originally published: 1984

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Cochlear Nuclear Complex
1.1 Innervation of Cochlear Nucleus
1.2 Parcellation of Cochlear Nucleus
1.3 Anteroventral Cochlear Nucleus
1.4 Posteroventral Cochlear Nucleus
1.5 Dorsal Cochlear Nucleus
2 Physiology of Cochlear Nucleus
2.1 Action Potential Wave Forms
2.2 Tonotopic Organization
2.3 Classification of Unit Discharge Patterns and Their Distributions
2.4 Tuning Curves
2.5 Responses as Function of Intensity
2.6 Phase Locking to Low‐Frequency Tones
2.7 Responses to Click Stimuli
2.8 Response Areas to Pure Tones and Effects of Anesthetic
2.9 Responses to Complex Stimuli
2.10 Morphology‐Physiology Correlations and Concept of Parallel Processing
3 Superior Olivary Complex
3.1 Anatomy of Superior Olivary Complex
3.2 Physiology of Superior Olivary Complex
3.3 null
4 Auditory Midbrain
4.1 Sources of Ascending Input to Inferior Colliculus
4.2 Nuclei of Lateral Lemniscus
5 Structure of Inferior Colliculus
5.1 Central Nucleus: Orientation and Lamination
5.2 Pericentral Nucleus
5.3 External Nucleus
6 Physiology and Organization of Inferior Colliculus
6.1 Representation of Cochlea Within Inferior Colliculus
6.2 Discharge Characteristics in Central Nucleus
6.3 Binaural Representation
6.4 Representation of Space
6.5 Organization According to Other Stimulus Dimensions
6.6 Discharge Characteristics in External and Pericentral Nuclei
6.7 Conclusions
7 Auditory Thalamus
7.1 Anatomy
7.2 Connections Between Auditory Midbrain and Thalamus
7.3 Physiological Studies of Units in Auditory Thalamus
7.4 Tonotopic Organization in Medial Geniculate Body
7.5 Distribution of Other Discharge Characteristics Within Ventral Division
7.6 Responses in Medial Division and Posterior Nuclear Group
7.7 Dorsal Division
7.8 Conclusions
8 Auditory Cortex
8.1 Introduction and Historical Background
8.2 Parcellation of Auditory Cortex and Tonotopic Organization
8.3 Fine Structure of Auditory Cortex
8.4 Connections with Thalamus
8.5 Centrifugal Connections
8.6 Corticocortical and Interhemispheric Connections
8.7 Neuronal Response Properties in Auditory Cortex
8.8 Behavioral Ablation Studies of Auditory Cortex Function
8.9 Acoustic Input to Association Cortex
8.10 Concluding Comments
9 General Conclusions
Figure 1. Figure 1.

Basic organization of ascending auditory pathway in mammals. For simplicity, only pathways to single cerebral hemisphere are shown. Auditory nerve bifurcates to terminate in dorsal and ventral cochlear nuclei (DCN and VCN, respectively). Several paths originate from this complex. Inputs from left and right cochlear nuclei converge on superior olivary complex (SOC) on each side, which in turn project via lateral lemniscus to midbrain auditory center, the inferior colliculus (IC). Other pathways from cochlear nuclei pass directly to contralateral IC via lateral lemniscus. Modest proportion of fibers in each of these pathways terminate in nuclei of lateral lemniscus (NLL). The IC projects bilaterally to auditory thalamus, medial geniculate body (MGB), by way of brachium of inferior colliculus. Finally, MGB projects to auditory cortical fields via auditory radiations. As figure indicates, each of major auditory centers comprises a number of subdivisions. Nature of these subdivisions and organization of their connections are described in greater detail in text and in subsequent figures.

Adapted from Merzenich and Kaas 292
Figure 2. Figure 2.

Parasagittal section through cochlear nucleus of 4‐day‐old cat stained by Golgi method. Auditory nerve fibers, AN, bifurcate to yield ascending branch to AVCN and descending branch to PVCN and DCN. Ascending branch terminates in AVCN with large end bulbs of Held.

From Lorente de Nó 279
Figure 3. Figure 3.

Cochlear nuclei in three dimensions showing bifurcation pattern in A, B: sagittal; C: transverse; and D: horizontal planes. Branches that represent high and low frequencies are labeled h and l, respectively. a.b., Ascending cochlear branch; a.v.c.n., anteroventral cochlear nucleus; C, caudal; co.f., cochlear nerve fiber; co. rest., restiform body; co. trap., trapezoid body; D, dorsal; d.b., descending cochlear branch; d.c.n., dorsal cochlear nucleus; gr.c.l., granular cell layer; m.l., molecular layer; L, lateral; M, medial; n.coch., cochlear nerve; n.vest., vestibular nerve; p.v.c.n., posteroventral cochlear nucleus; R, rostral; str.ac., acoustic striae; tr.sp.n.V., spinal fifth tract; V, ventral.

From Osen 346
Figure 4. Figure 4.

Schematic drawings of sagittal sections comparing A: divisions of cochlear nucleus identified by Brawer et al. 59, and B: divisions of cochlear nucleus of Osen 343. In A: AVCN, anterior ventral cochlear nucleus, which is divided into anterior division comprising AA, anterior; AP, posterior; and APD, dorsal parts; and a posterior division comprising PD, dorsal; and PV, ventral parts; PVCN, posterior ventral cochlear nucleus; G, granule cell layer; DCN, dorsal cochlear nucleus; dotted line represents position of fusiform (pyramidal) cell layer. In B: nvea, vestibular nerve; oca, octopus cell area; cap, small cell cap; crdcn, central region of dorsal cochlear nucleus; ab, ascending cochlear branch; cof, cochlear nerve fiber; db, descending cochlear branch; ml, molecular layer.
Figure 5. Figure 5.

Sagittal section of cochlear nucleus with superimposed electrode track (thionine stain), caudal and rostral to left and right, respectively. Major subdivisions in dorsal (DCN) and antero‐(AVN) and postero‐(PVN) ventral cochlear nuclei indicated by interrupted lines. Incoming cochlear fibers indicated by cn and arrow. Solid lines and crossbars indicate electrode track and depth from dorsal surface in millimeters. Top: plotted sequence of characteristic frequencies (CFs) from 21 units. First CF sequence of 8 units recorded in DCN, second recorded in AVN; both have been fitted with straight lines. Note increase in CF when electrode passes from DCN to AVN.

From Evans 133
Figure 6. Figure 6.

Outline of cochlear nuclei from computer graphics showing iso‐characteristic frequency sheets in anteroventral cochlear nucleus (AVCN) in three dimensions (A: transverse; B: horizontal; C: sagittal). Lines labeled with numbers indicate CF sheets. GCL, granular cell layer; A, anterior; D, dorsal; L, lateral; M, medial; P, posterior; V, ventral; AVCN, anterior ventral cochlear nucleus, which is divided into anterior division comprising AA, anterior; AP, posterior; and APD, dorsal parts; and a posterior division comprising PD, dorsal; and PV, ventral parts; PVCN, posterior ventral cochlear nucleus; DCN, dorsal cochlear nucleus.
Figure 7. Figure 7.

Schematic sagittal section showing frequency distributions of Pfeiffer 356 characteristic frequency types recorded from various subdivisions of cochlear nuclei. Top row shows discharge pattern types from left to right: primarylike (diagonal lines); choppers (dots); on (cross hatch); pauser or buildup (horizontal lines). AVCN, anterior ventral cochlear nucleus divided into anterior division comprising AA, anterior; AP, posterior; and APD, dorsal parts; and a posterior division comprising PD, dorsal; and PV, ventral parts; PVCN, posterior ventral cochlear nucleus; A‐PVCN, anterior part of PVCN; C‐PVCN, central part of PVCN, also octopus cell area; P‐PVCN, posterior part of PVCN; DCN, dorsal cochlear nucleus; C‐DCN, polymorphic or deep layer of DCN; F‐DCN, fusiform or pyramidal cell layer of DCN.

From Tsuchitani 452
Figure 8. Figure 8.

Discharge characteristics for unit in dorsal cochlear nucleus (chloralose anesthesia). A: excitatory tuning curve (stippled); inhibitory tuning curve, CF, and inhibitory sidebands are cross hatched. B‐D: three‐dimensional arrays of poststimulus time histograms ordered in frequency (6–24 kHz) and intensity (10, 20, and 30 dB above threshold, respectively, as indicated in A). Tone burst (0.4 s) indicated by bar and interrupted lines; ordinate, firing rate in spikes/s. Note extensive “sea” of inhibition in D with narrow band (“island”) of delayed excitation at 21 kHz.

From Evans 133
Figure 9. Figure 9.

Discharge characteristics of dorsal cochlear nucleus unit with an entirely inhibitory characteristic frequency (unanesthetized decerebrate cat). A: Tuning curve. B: Three‐dimensional array of poststimulus time histograms to 0.4‐s tone (bar) at 25 dB above threshold. Note inhibition of spontaneous activity during and following tone. Ordinate: firing rate in spikes/s.

From Evans 133
Figure 10. Figure 10.

Montage of poststimulus time histograms showing response area of chopper unit (R75‐39‐9) recorded in posteroventral cochlear nucleus of rabbit. Stimuli were 25‐ms tone bursts presented at 10/s. Rise and fall times of stimulus were each 1.5 ms. Frequency range is from 10 to 20 kHz in steps of 1.0 kHz, shown above each histogram. Intensity levels from bottom row upwards are 20, 40, 60, 80 dB sound pressure level shown at left. Insert: isointensity curves indicating the number of spikes per tone burst. (Based on unpublished data of D. R. Perry and W. R. Webster).
Figure 11. Figure 11.

Schematic diagram of projections of cochlear nucleus to superior olivary complex and higher centers in cat, showing projections of some CN cell types, mso, Medial superior olive; lso, lateral superior olive; mntb, medial nucleus of trapezoid body; vntb, ventral nucleus of trapezoid body; lntb, lateral nucleus of trapezoid body; dmpo, dorsomedial periolivary nucleus; dlpo, dorsolateral periolivary nucleus; OCB, olivocochlear bundle; LLD, dorsal nucleus of lateral lemniscus; LLV, ventral nucleus of lateral lemniscus; lat. lemn, lateral lemniscus; cent. nuc. inf. coll., central nucleus of inferior colliculus; dors. ac. str., dorsal acoustic stria; interm. ac. str., intermediate acoustic stria.

Adapted from Moore and Osen 310
Figure 12. Figure 12.

Representation of terminal plexes in pontine auditory nuclei, stained by Golgi technique (2‐day‐old cat, transverse section). Large calyces of Held can be seen in MNTB (right). Insert: location of superior olivary nuclei. DPO, dorsal periolivary nucleus; DLPO, dorsolateral periolivary nucleus; DMPO, dorsomedial periolivary nucleus; VMPO, ventromedial periolivary nucleus; VLPO, ventrolateral periolivary nucleus; MSO, medial superior olive; LSO, lateral superior olive; LNTB, lateral nucleus of trapezoid body; MNTB, medial nucleus of trapezoid body; VNTB, ventral nucleus of trapezoid body.

From Tsuchitani 452
Figure 13. Figure 13.

Discharge rate and vector strength (a measure of degree of phase locking) plotted as function of interaural delay for a phase‐sensitive unit recorded in medial superior olive of beagle 169. Stimulus was best frequency tone of 444.5 Hz at 70 dB. Note that maximum discharge rate and maximum phase locking occur at same interaural delay. Points on left are discharge rates for contralateral, C, and ipsilateral, I, monaural stimuli and spontaneous level, NS.

From Goldberg and Brown 169
Figure 14. Figure 14.

Nissl‐stained frontal section through midbrain of cat, showing principal nuclei comprising auditory midbrain. Uniformly darkly stained cells of central nucleus of inferior colliculus, ICC, are flanked dorsally by smaller densely packed neurons of pericentral nucleus, ICP, whose cells mingle medially with fibers of commissure of inferior colliculus, ICO. A gradation in cytoarchitecture laterally corresponds to external nucleus, ICX, ventral to which lies a small pocket of densely packed neurons, nucleus sagulum, SAG. Two principal cell masses of nuclei of lateral lemniscus, dorsal, LLD, and ventral, LLV, are separated by intermediate zone containing few cells among many fibers of lateral lemniscus.
Figure 15. Figure 15.

Sequences of single‐unit characteristic frequencies recorded in A: dorsal‐to‐ventral, and B: caudal‐to‐rostral penetration through cat inferior colliculus shown schematically in sagittal plane. In A, CFs are listed at right of histological outline; in B: each unit is represented as a symbol on the graph relating caudal, C, to rostral, R, penetration distance in mm against CF in kHz. Different symbols refer to different binaural classes: filled circles, EI cells; open circles, EO cells; triangles, interaural time delay cells (see text for details). SP, distance from midline in mm; ICC, ICP, ICX, central, pericentral, and external nuclei of inferior colliculus, respectively; LLD, LLV, dorsal and ventral nuclei of lateral lemniscus; SCS, SCI, superficial and intermediate layers of superior colliculus; BC, brachium conjunctivum; T5, track number 5 in this cat. Pentobarbital anesthesia. (Based on unpublished data of M. N. Semple.)
Figure 16. Figure 16.

A: autoradiograph, and B: Nissl stain of same frontal section through cat inferior colliculus. Tone pips of 54 dB sound pressure level alternating in frequency (1 kHz, 250 ms; 100 ms pause; 8 kHz, 250 ms) were presented for 45 min to cochlea contralateral to inferior colliculus labeled in A (pentobarbital anesthesia). An intravenous injection of 2‐[14C]deoxyglucose (200 μCi/kg) was made at beginning of stimulation period. (Based on unpublished work of W. R. Webster and J. Servière.)
Figure 17. Figure 17.

Comparison of density of projections to central nucleus of inferior colliculus from selected ipsilateral (IPSI, left column) and contralateral (CONTRA, right column) brain stem auditory nuclei. MSO, LSO, DCN, medial and lateral superior olives and dorsal cochlear nucleus, respectively. An 0.5 μl injection of 30% HRP was made in lateral part of central nucleus of cat, and sections were cut in frontal plane at 90 μm, and every second section was reacted for HRP. All HRP‐labeled cells were counted in each of above nuclei in every section where they occurred. Counts for each section are given on ordinates; locations of section along relative rostral, R,‐to‐caudal, C, dimensions of each nucleus in mm are given on abscissas. Note that, for simplicity, each count is binned in 180μm bins because each 90‐μm HRP‐reacted section was separated from next by a 90‐μm unreacted Nissl‐stained section. Total R‐C thickness of each nucleus is shown as horizontal line at zero count level at base of each histogram. N, total number of labeled cells comprising each histogram.
Figure 18. Figure 18.

Characteristic frequency plotted as function of relative unit depth for dorsal‐to‐ventral penetrations in tonotopic region (top), transitional region (middle), and space‐mapped region (bottom) of MLD, auditory midbrain of barn owl. Unit depths measured with respect to first MLD unit encountered in each penetration. Each symbol signifies units from a single penetration, approximate location of which is indicated on right in diagram of horizontal section through optic lobe. Orientation of horizontal section indicated by crossed arrows. a, Anterior, p, posterior; l, lateral; m, medial; OT, optic tectum.

From Knudsen and Konishi 496
Figure 19. Figure 19.

Representation of auditory space in MLD, auditory midbrain of barn owl, as defined by centers of unit best areas. In upper left, coordinates of frontal hemisphere of auditory space are depicted as dotted globe surrounding owl. Elevations shown in relation to horizontal plane of owl's head—e.g., +30 (30° above horizontal plane). Azimuths shown in relation to interaural line, and MLD recorded from—e.g., 30c (30° from 0° azimuth in quadrant contralateral to MLD being studied); 20i (20° in ipsilateral field). Projected onto globe are best areas (solid‐line rectangles) of 14 units recorded in four separate penetrations. Large numbers backed by similar symbols represent units from same penetration; numbers themselves signify order in which units were encountered and are placed at centers of their best areas. Penetrations made with electrode oriented parallel to transverse plane at positions indicated in horizontal section by solid arrows. Below and to right of globe are three histological sections through MLD in horizontal, transverse, and sagittal planes. Stippled portion of MLD corresponds to space‐mapped region; remaining portion is tonotopic region. Isoazimuth contours, based on best‐area centers, shown as solid lines in horizontal and sagittal sections; isoelevation contours represented by dashed lines in transverse and sagittal sections. On each section, dashed arrows indicate planes of other two sections. Solid, crossed arrows at lower right of each section define orientation of section. a, Anterior; d, dorsal; l, lateral; m, medial; p, posterior; v, ventral; OT, optic tectum.

From Knudsen and Konishi 258. Copyright 1978 by the American Association for the Advancement of Science
Figure 20. Figure 20.

Major divisions of medial geniculate body, MGB, as defined by principal neuron types described in text. Transverse section (Golgi‐Cox) at junction of anterior and middle thirds of MGB. BCS, brachium of superior colliculus; CGL, lateral geniculate body; DP, deep dorsal nucleus of MGB; DS, superficial dorsal nucleus of MGB; LM, medial lemniscus; LV, pars lateralis of ventral division of MGB; M, medial division of MGB; NS, suprageniculate nucleus; PC, cerebral peduncle; TO, optic tract; TS, spinothalamic tract; VL, ventrolateral nucleus of MGB; VPL, thalamic ventral posterolateral nucleus; X, subnucleus, thalamic lateral posterior nucleus; ZM, marginal zone of MGB.

From Morest 315
Figure 21. Figure 21.

Schematic sagittal sections (dorsal, top; rostral, left) of cat showing micropipette recording and HRP electrophoresis sites in medial geniculate body (upper) and locations of HRP‐labeled cells in inferior colliculus (lower). A, B, C: three different experiments in which HRP has been effluxed between unit recording sites with stated best frequencies. M, number of millimeters medial to lateral surface of medial geniculate body; 5.0‐6.0, etc, distance of inferior colliculus sections from midline in mm. Calibration applied to all sections. ICC and ICP, central and pericentral nuclei of inferior colliculus, respectively. (Based on unpublished work of L. M. Aitkin and M. B. Calford.)
Figure 22. Figure 22.

Three parallel micropipette tracks with associated best frequency and binaural data on one cat. Schematic sagittal section through caudal thalamus (caudal to right) 2.5 mm from lateral edge of medial geniculate body (MGB). LGn, lateral geniculate nucleus; BIC, brachium of inferior colliculus; LV, OV, pars lateralis and pars ovoidea of ventral MGB; D, dorsal division of MGB. EE, EE*, units for which stimuli to each ear (convention: contra effect shown first) cause excitation, with asterisk denoting stronger response in terms of either spike count at given intensity or threshold; EI, contralateral stimuli excite, ipsilateral stimuli inhibit; EI*, threshold for ipsi inhibitory effect lower than for contra excitatory effect; EO, monaural contralateral excitatory input only; B, broadly tuned.

Adapted from Calford and Webster 77
Figure 23. Figure 23.

Auditory cortical fields in cat. A: parcellation proposed by Woolsey 487 in 1960, showing cortical fields (AI, AII, EP, SF, INS, and AIII) described in text. In each field, orientation of cochlear representation is indicated by position of A (apex) and B (base). Auditory responses also recorded in association areas on suprasylvian and anterior lateral gyri (ASSOC.) and in pericruciate sensorimotor cortex (MI). Long‐latency (LATE) responses are recorded in visual cortex. B, C: parcellation into four tonotopic (AI, A, P, and VP) and additional belt fields (AII, DP, V, and T) described by Reale and Imig 376. Because location of physiologically determined field boundaries in different animals varies with respect to sulci, positions shown are general approximations only. In B, field positions are shown relative to sulci on a lateral view of surface of left cerebral hemisphere; sss: suprasylvian sulcus; aes: anterior ectosylvian sulcus; pes: posterior ectosylvian sulcus; pss: pseudosylvian sulcus. In C, unfolded cortical surface forming gyral surfaces and sulcal banks in unshaded region in B is shown. Cortical surfaces forming sulcal banks are shaded, whereas those forming gyral surfaces are not. Tonotopic fields are delimited by heavy broken lines, and locations of highest and lowest best frequencies in these fields are indicated by low and high, respectively.

A: from Woolsey 487; B, C: from Imig and Reale 216
Figure 24. Figure 24.

A, B: Surface maps showing distribution of characteristic frequencies (CF) determined within parallel electrode penetrations (66 in A; 57 in B) into auditory cortex. Sites of electrode penetrations represented by dots in inset brain photographs. Each number in drawings is CF (in kHz) of neurons encountered within a penetration at that site. Dashed lines are approximately parallel to isofrequency contours. Stars represent electrode penetrations in which auditory responses were encountered, but in which no CF determination could be made.

From Merzenich et al. 294
Figure 25. Figure 25.

Characteristic frequency as a function of distance across cortical surface in AI of cat. Each graph (A, B, C, D1, and D2) is derived from an individual cortical map of type presented in Fig. 24. Ordinate is distance on cortical surface on axis perpendicular to cortical isofrequency contours. Distance measured from straight line caudal to mapped cortical surface and parallel to straight‐line approximations of isofrequency contours. Data in graph A derived from points along six parallel lines spanning entire mapped sector of AI; graphs in B and C based on five parallel lines, and those in D1 and D2 on four parallel lines. In each case, data points from different lines are represented by different symbols.

From Merzenich et al. 294
Figure 26. Figure 26.

Topographic organization of auditory corticocortical connections in cat as revealed by combined electrophysiological and anatomical tracing studies. Tonotopic maps of cortical fields were obtained by microelectrode mapping procedures, and distribution of axon terminals within a field was determined by autoradiographic labeling with tritiated proline and leucine. A, B: graphs showing relationship between range of best frequencies in central region of injection zone in AI (graph A) or field A (graph B), and range of best frequencies in labeled regions of target fields A, AI, V, or VP. Each rectangle represents a projection to a target field: horizontal side represents range of best frequencies in central region of injection zone (abscissa); vertical side represents range of best frequencies in labeled portion of target field. Letter associated with each rectangle identifies target field; subscript c indicates projections to fields in hemisphere contralateral to injection site.

From Imig and Reale 216
Figure 27. Figure 27.

Functions showing sensitivity to interaural intensity differences (IID) for five representative neurons in physiologically defined AI of anesthetized cat. Interaural intensity differences are generated by varying contralateral and ipsilateral intensities symmetrically around average binaural intensity of 50–60 dB sound pressure level. Note that in each case neuron responds maximally over range of IIDs for which contralateral intensity exceeds ipsilateral (corresponding to contralateral azimuths), and that response strength declines sharply over limited IID range. Functions for individual neurons differ in location of cutoff; it has not yet been determined whether variation in position of cutoff is a systematic function of neural place, either in cortex or in any subcortical structure (but see ref. 484).

From unpublished data of D. P. Phillips and D. R. F. Irvine


Figure 1.

Basic organization of ascending auditory pathway in mammals. For simplicity, only pathways to single cerebral hemisphere are shown. Auditory nerve bifurcates to terminate in dorsal and ventral cochlear nuclei (DCN and VCN, respectively). Several paths originate from this complex. Inputs from left and right cochlear nuclei converge on superior olivary complex (SOC) on each side, which in turn project via lateral lemniscus to midbrain auditory center, the inferior colliculus (IC). Other pathways from cochlear nuclei pass directly to contralateral IC via lateral lemniscus. Modest proportion of fibers in each of these pathways terminate in nuclei of lateral lemniscus (NLL). The IC projects bilaterally to auditory thalamus, medial geniculate body (MGB), by way of brachium of inferior colliculus. Finally, MGB projects to auditory cortical fields via auditory radiations. As figure indicates, each of major auditory centers comprises a number of subdivisions. Nature of these subdivisions and organization of their connections are described in greater detail in text and in subsequent figures.

Adapted from Merzenich and Kaas 292


Figure 2.

Parasagittal section through cochlear nucleus of 4‐day‐old cat stained by Golgi method. Auditory nerve fibers, AN, bifurcate to yield ascending branch to AVCN and descending branch to PVCN and DCN. Ascending branch terminates in AVCN with large end bulbs of Held.

From Lorente de Nó 279


Figure 3.

Cochlear nuclei in three dimensions showing bifurcation pattern in A, B: sagittal; C: transverse; and D: horizontal planes. Branches that represent high and low frequencies are labeled h and l, respectively. a.b., Ascending cochlear branch; a.v.c.n., anteroventral cochlear nucleus; C, caudal; co.f., cochlear nerve fiber; co. rest., restiform body; co. trap., trapezoid body; D, dorsal; d.b., descending cochlear branch; d.c.n., dorsal cochlear nucleus; gr.c.l., granular cell layer; m.l., molecular layer; L, lateral; M, medial; n.coch., cochlear nerve; n.vest., vestibular nerve; p.v.c.n., posteroventral cochlear nucleus; R, rostral; str.ac., acoustic striae; tr.sp.n.V., spinal fifth tract; V, ventral.

From Osen 346


Figure 4.

Schematic drawings of sagittal sections comparing A: divisions of cochlear nucleus identified by Brawer et al. 59, and B: divisions of cochlear nucleus of Osen 343. In A: AVCN, anterior ventral cochlear nucleus, which is divided into anterior division comprising AA, anterior; AP, posterior; and APD, dorsal parts; and a posterior division comprising PD, dorsal; and PV, ventral parts; PVCN, posterior ventral cochlear nucleus; G, granule cell layer; DCN, dorsal cochlear nucleus; dotted line represents position of fusiform (pyramidal) cell layer. In B: nvea, vestibular nerve; oca, octopus cell area; cap, small cell cap; crdcn, central region of dorsal cochlear nucleus; ab, ascending cochlear branch; cof, cochlear nerve fiber; db, descending cochlear branch; ml, molecular layer.



Figure 5.

Sagittal section of cochlear nucleus with superimposed electrode track (thionine stain), caudal and rostral to left and right, respectively. Major subdivisions in dorsal (DCN) and antero‐(AVN) and postero‐(PVN) ventral cochlear nuclei indicated by interrupted lines. Incoming cochlear fibers indicated by cn and arrow. Solid lines and crossbars indicate electrode track and depth from dorsal surface in millimeters. Top: plotted sequence of characteristic frequencies (CFs) from 21 units. First CF sequence of 8 units recorded in DCN, second recorded in AVN; both have been fitted with straight lines. Note increase in CF when electrode passes from DCN to AVN.

From Evans 133


Figure 6.

Outline of cochlear nuclei from computer graphics showing iso‐characteristic frequency sheets in anteroventral cochlear nucleus (AVCN) in three dimensions (A: transverse; B: horizontal; C: sagittal). Lines labeled with numbers indicate CF sheets. GCL, granular cell layer; A, anterior; D, dorsal; L, lateral; M, medial; P, posterior; V, ventral; AVCN, anterior ventral cochlear nucleus, which is divided into anterior division comprising AA, anterior; AP, posterior; and APD, dorsal parts; and a posterior division comprising PD, dorsal; and PV, ventral parts; PVCN, posterior ventral cochlear nucleus; DCN, dorsal cochlear nucleus.



Figure 7.

Schematic sagittal section showing frequency distributions of Pfeiffer 356 characteristic frequency types recorded from various subdivisions of cochlear nuclei. Top row shows discharge pattern types from left to right: primarylike (diagonal lines); choppers (dots); on (cross hatch); pauser or buildup (horizontal lines). AVCN, anterior ventral cochlear nucleus divided into anterior division comprising AA, anterior; AP, posterior; and APD, dorsal parts; and a posterior division comprising PD, dorsal; and PV, ventral parts; PVCN, posterior ventral cochlear nucleus; A‐PVCN, anterior part of PVCN; C‐PVCN, central part of PVCN, also octopus cell area; P‐PVCN, posterior part of PVCN; DCN, dorsal cochlear nucleus; C‐DCN, polymorphic or deep layer of DCN; F‐DCN, fusiform or pyramidal cell layer of DCN.

From Tsuchitani 452


Figure 8.

Discharge characteristics for unit in dorsal cochlear nucleus (chloralose anesthesia). A: excitatory tuning curve (stippled); inhibitory tuning curve, CF, and inhibitory sidebands are cross hatched. B‐D: three‐dimensional arrays of poststimulus time histograms ordered in frequency (6–24 kHz) and intensity (10, 20, and 30 dB above threshold, respectively, as indicated in A). Tone burst (0.4 s) indicated by bar and interrupted lines; ordinate, firing rate in spikes/s. Note extensive “sea” of inhibition in D with narrow band (“island”) of delayed excitation at 21 kHz.

From Evans 133


Figure 9.

Discharge characteristics of dorsal cochlear nucleus unit with an entirely inhibitory characteristic frequency (unanesthetized decerebrate cat). A: Tuning curve. B: Three‐dimensional array of poststimulus time histograms to 0.4‐s tone (bar) at 25 dB above threshold. Note inhibition of spontaneous activity during and following tone. Ordinate: firing rate in spikes/s.

From Evans 133


Figure 10.

Montage of poststimulus time histograms showing response area of chopper unit (R75‐39‐9) recorded in posteroventral cochlear nucleus of rabbit. Stimuli were 25‐ms tone bursts presented at 10/s. Rise and fall times of stimulus were each 1.5 ms. Frequency range is from 10 to 20 kHz in steps of 1.0 kHz, shown above each histogram. Intensity levels from bottom row upwards are 20, 40, 60, 80 dB sound pressure level shown at left. Insert: isointensity curves indicating the number of spikes per tone burst. (Based on unpublished data of D. R. Perry and W. R. Webster).



Figure 11.

Schematic diagram of projections of cochlear nucleus to superior olivary complex and higher centers in cat, showing projections of some CN cell types, mso, Medial superior olive; lso, lateral superior olive; mntb, medial nucleus of trapezoid body; vntb, ventral nucleus of trapezoid body; lntb, lateral nucleus of trapezoid body; dmpo, dorsomedial periolivary nucleus; dlpo, dorsolateral periolivary nucleus; OCB, olivocochlear bundle; LLD, dorsal nucleus of lateral lemniscus; LLV, ventral nucleus of lateral lemniscus; lat. lemn, lateral lemniscus; cent. nuc. inf. coll., central nucleus of inferior colliculus; dors. ac. str., dorsal acoustic stria; interm. ac. str., intermediate acoustic stria.

Adapted from Moore and Osen 310


Figure 12.

Representation of terminal plexes in pontine auditory nuclei, stained by Golgi technique (2‐day‐old cat, transverse section). Large calyces of Held can be seen in MNTB (right). Insert: location of superior olivary nuclei. DPO, dorsal periolivary nucleus; DLPO, dorsolateral periolivary nucleus; DMPO, dorsomedial periolivary nucleus; VMPO, ventromedial periolivary nucleus; VLPO, ventrolateral periolivary nucleus; MSO, medial superior olive; LSO, lateral superior olive; LNTB, lateral nucleus of trapezoid body; MNTB, medial nucleus of trapezoid body; VNTB, ventral nucleus of trapezoid body.

From Tsuchitani 452


Figure 13.

Discharge rate and vector strength (a measure of degree of phase locking) plotted as function of interaural delay for a phase‐sensitive unit recorded in medial superior olive of beagle 169. Stimulus was best frequency tone of 444.5 Hz at 70 dB. Note that maximum discharge rate and maximum phase locking occur at same interaural delay. Points on left are discharge rates for contralateral, C, and ipsilateral, I, monaural stimuli and spontaneous level, NS.

From Goldberg and Brown 169


Figure 14.

Nissl‐stained frontal section through midbrain of cat, showing principal nuclei comprising auditory midbrain. Uniformly darkly stained cells of central nucleus of inferior colliculus, ICC, are flanked dorsally by smaller densely packed neurons of pericentral nucleus, ICP, whose cells mingle medially with fibers of commissure of inferior colliculus, ICO. A gradation in cytoarchitecture laterally corresponds to external nucleus, ICX, ventral to which lies a small pocket of densely packed neurons, nucleus sagulum, SAG. Two principal cell masses of nuclei of lateral lemniscus, dorsal, LLD, and ventral, LLV, are separated by intermediate zone containing few cells among many fibers of lateral lemniscus.



Figure 15.

Sequences of single‐unit characteristic frequencies recorded in A: dorsal‐to‐ventral, and B: caudal‐to‐rostral penetration through cat inferior colliculus shown schematically in sagittal plane. In A, CFs are listed at right of histological outline; in B: each unit is represented as a symbol on the graph relating caudal, C, to rostral, R, penetration distance in mm against CF in kHz. Different symbols refer to different binaural classes: filled circles, EI cells; open circles, EO cells; triangles, interaural time delay cells (see text for details). SP, distance from midline in mm; ICC, ICP, ICX, central, pericentral, and external nuclei of inferior colliculus, respectively; LLD, LLV, dorsal and ventral nuclei of lateral lemniscus; SCS, SCI, superficial and intermediate layers of superior colliculus; BC, brachium conjunctivum; T5, track number 5 in this cat. Pentobarbital anesthesia. (Based on unpublished data of M. N. Semple.)



Figure 16.

A: autoradiograph, and B: Nissl stain of same frontal section through cat inferior colliculus. Tone pips of 54 dB sound pressure level alternating in frequency (1 kHz, 250 ms; 100 ms pause; 8 kHz, 250 ms) were presented for 45 min to cochlea contralateral to inferior colliculus labeled in A (pentobarbital anesthesia). An intravenous injection of 2‐[14C]deoxyglucose (200 μCi/kg) was made at beginning of stimulation period. (Based on unpublished work of W. R. Webster and J. Servière.)



Figure 17.

Comparison of density of projections to central nucleus of inferior colliculus from selected ipsilateral (IPSI, left column) and contralateral (CONTRA, right column) brain stem auditory nuclei. MSO, LSO, DCN, medial and lateral superior olives and dorsal cochlear nucleus, respectively. An 0.5 μl injection of 30% HRP was made in lateral part of central nucleus of cat, and sections were cut in frontal plane at 90 μm, and every second section was reacted for HRP. All HRP‐labeled cells were counted in each of above nuclei in every section where they occurred. Counts for each section are given on ordinates; locations of section along relative rostral, R,‐to‐caudal, C, dimensions of each nucleus in mm are given on abscissas. Note that, for simplicity, each count is binned in 180μm bins because each 90‐μm HRP‐reacted section was separated from next by a 90‐μm unreacted Nissl‐stained section. Total R‐C thickness of each nucleus is shown as horizontal line at zero count level at base of each histogram. N, total number of labeled cells comprising each histogram.



Figure 18.

Characteristic frequency plotted as function of relative unit depth for dorsal‐to‐ventral penetrations in tonotopic region (top), transitional region (middle), and space‐mapped region (bottom) of MLD, auditory midbrain of barn owl. Unit depths measured with respect to first MLD unit encountered in each penetration. Each symbol signifies units from a single penetration, approximate location of which is indicated on right in diagram of horizontal section through optic lobe. Orientation of horizontal section indicated by crossed arrows. a, Anterior, p, posterior; l, lateral; m, medial; OT, optic tectum.

From Knudsen and Konishi 496


Figure 19.

Representation of auditory space in MLD, auditory midbrain of barn owl, as defined by centers of unit best areas. In upper left, coordinates of frontal hemisphere of auditory space are depicted as dotted globe surrounding owl. Elevations shown in relation to horizontal plane of owl's head—e.g., +30 (30° above horizontal plane). Azimuths shown in relation to interaural line, and MLD recorded from—e.g., 30c (30° from 0° azimuth in quadrant contralateral to MLD being studied); 20i (20° in ipsilateral field). Projected onto globe are best areas (solid‐line rectangles) of 14 units recorded in four separate penetrations. Large numbers backed by similar symbols represent units from same penetration; numbers themselves signify order in which units were encountered and are placed at centers of their best areas. Penetrations made with electrode oriented parallel to transverse plane at positions indicated in horizontal section by solid arrows. Below and to right of globe are three histological sections through MLD in horizontal, transverse, and sagittal planes. Stippled portion of MLD corresponds to space‐mapped region; remaining portion is tonotopic region. Isoazimuth contours, based on best‐area centers, shown as solid lines in horizontal and sagittal sections; isoelevation contours represented by dashed lines in transverse and sagittal sections. On each section, dashed arrows indicate planes of other two sections. Solid, crossed arrows at lower right of each section define orientation of section. a, Anterior; d, dorsal; l, lateral; m, medial; p, posterior; v, ventral; OT, optic tectum.

From Knudsen and Konishi 258. Copyright 1978 by the American Association for the Advancement of Science


Figure 20.

Major divisions of medial geniculate body, MGB, as defined by principal neuron types described in text. Transverse section (Golgi‐Cox) at junction of anterior and middle thirds of MGB. BCS, brachium of superior colliculus; CGL, lateral geniculate body; DP, deep dorsal nucleus of MGB; DS, superficial dorsal nucleus of MGB; LM, medial lemniscus; LV, pars lateralis of ventral division of MGB; M, medial division of MGB; NS, suprageniculate nucleus; PC, cerebral peduncle; TO, optic tract; TS, spinothalamic tract; VL, ventrolateral nucleus of MGB; VPL, thalamic ventral posterolateral nucleus; X, subnucleus, thalamic lateral posterior nucleus; ZM, marginal zone of MGB.

From Morest 315


Figure 21.

Schematic sagittal sections (dorsal, top; rostral, left) of cat showing micropipette recording and HRP electrophoresis sites in medial geniculate body (upper) and locations of HRP‐labeled cells in inferior colliculus (lower). A, B, C: three different experiments in which HRP has been effluxed between unit recording sites with stated best frequencies. M, number of millimeters medial to lateral surface of medial geniculate body; 5.0‐6.0, etc, distance of inferior colliculus sections from midline in mm. Calibration applied to all sections. ICC and ICP, central and pericentral nuclei of inferior colliculus, respectively. (Based on unpublished work of L. M. Aitkin and M. B. Calford.)



Figure 22.

Three parallel micropipette tracks with associated best frequency and binaural data on one cat. Schematic sagittal section through caudal thalamus (caudal to right) 2.5 mm from lateral edge of medial geniculate body (MGB). LGn, lateral geniculate nucleus; BIC, brachium of inferior colliculus; LV, OV, pars lateralis and pars ovoidea of ventral MGB; D, dorsal division of MGB. EE, EE*, units for which stimuli to each ear (convention: contra effect shown first) cause excitation, with asterisk denoting stronger response in terms of either spike count at given intensity or threshold; EI, contralateral stimuli excite, ipsilateral stimuli inhibit; EI*, threshold for ipsi inhibitory effect lower than for contra excitatory effect; EO, monaural contralateral excitatory input only; B, broadly tuned.

Adapted from Calford and Webster 77


Figure 23.

Auditory cortical fields in cat. A: parcellation proposed by Woolsey 487 in 1960, showing cortical fields (AI, AII, EP, SF, INS, and AIII) described in text. In each field, orientation of cochlear representation is indicated by position of A (apex) and B (base). Auditory responses also recorded in association areas on suprasylvian and anterior lateral gyri (ASSOC.) and in pericruciate sensorimotor cortex (MI). Long‐latency (LATE) responses are recorded in visual cortex. B, C: parcellation into four tonotopic (AI, A, P, and VP) and additional belt fields (AII, DP, V, and T) described by Reale and Imig 376. Because location of physiologically determined field boundaries in different animals varies with respect to sulci, positions shown are general approximations only. In B, field positions are shown relative to sulci on a lateral view of surface of left cerebral hemisphere; sss: suprasylvian sulcus; aes: anterior ectosylvian sulcus; pes: posterior ectosylvian sulcus; pss: pseudosylvian sulcus. In C, unfolded cortical surface forming gyral surfaces and sulcal banks in unshaded region in B is shown. Cortical surfaces forming sulcal banks are shaded, whereas those forming gyral surfaces are not. Tonotopic fields are delimited by heavy broken lines, and locations of highest and lowest best frequencies in these fields are indicated by low and high, respectively.

A: from Woolsey 487; B, C: from Imig and Reale 216


Figure 24.

A, B: Surface maps showing distribution of characteristic frequencies (CF) determined within parallel electrode penetrations (66 in A; 57 in B) into auditory cortex. Sites of electrode penetrations represented by dots in inset brain photographs. Each number in drawings is CF (in kHz) of neurons encountered within a penetration at that site. Dashed lines are approximately parallel to isofrequency contours. Stars represent electrode penetrations in which auditory responses were encountered, but in which no CF determination could be made.

From Merzenich et al. 294


Figure 25.

Characteristic frequency as a function of distance across cortical surface in AI of cat. Each graph (A, B, C, D1, and D2) is derived from an individual cortical map of type presented in Fig. 24. Ordinate is distance on cortical surface on axis perpendicular to cortical isofrequency contours. Distance measured from straight line caudal to mapped cortical surface and parallel to straight‐line approximations of isofrequency contours. Data in graph A derived from points along six parallel lines spanning entire mapped sector of AI; graphs in B and C based on five parallel lines, and those in D1 and D2 on four parallel lines. In each case, data points from different lines are represented by different symbols.

From Merzenich et al. 294


Figure 26.

Topographic organization of auditory corticocortical connections in cat as revealed by combined electrophysiological and anatomical tracing studies. Tonotopic maps of cortical fields were obtained by microelectrode mapping procedures, and distribution of axon terminals within a field was determined by autoradiographic labeling with tritiated proline and leucine. A, B: graphs showing relationship between range of best frequencies in central region of injection zone in AI (graph A) or field A (graph B), and range of best frequencies in labeled regions of target fields A, AI, V, or VP. Each rectangle represents a projection to a target field: horizontal side represents range of best frequencies in central region of injection zone (abscissa); vertical side represents range of best frequencies in labeled portion of target field. Letter associated with each rectangle identifies target field; subscript c indicates projections to fields in hemisphere contralateral to injection site.

From Imig and Reale 216


Figure 27.

Functions showing sensitivity to interaural intensity differences (IID) for five representative neurons in physiologically defined AI of anesthetized cat. Interaural intensity differences are generated by varying contralateral and ipsilateral intensities symmetrically around average binaural intensity of 50–60 dB sound pressure level. Note that in each case neuron responds maximally over range of IIDs for which contralateral intensity exceeds ipsilateral (corresponding to contralateral azimuths), and that response strength declines sharply over limited IID range. Functions for individual neurons differ in location of cutoff; it has not yet been determined whether variation in position of cutoff is a systematic function of neural place, either in cortex or in any subcortical structure (but see ref. 484).

From unpublished data of D. P. Phillips and D. R. F. Irvine
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Article Title: Central Neural Mechanisms of Hearing
 

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L. M. Aitkin, D. R. F. Irvine, W. R. Webster. Central Neural Mechanisms of Hearing. Compr Physiol 2011, Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes: 675-737. First published in print 1984. doi: 10.1002/cphy.cp010316