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Emotion

Joseph E. LeDoux

10.1002/cphy.cp010510

Source: Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain

Originally published: 1987

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 What is Emotion?
2 Brain and Emotion: Historical Landmarks
2.1 Sham Rage
2.2 Papez Circuit
2.3 Psychic Blindness
2.4 Visceral Brain and Limbic System
3 Organization of Limbic Forebrain
3.1 Current Status of Limbic System Concept
3.2 Basic Circuits of Limbic Forebrain
4 Emotional Evaluation: Central Coding of Stimulus Significance
4.1 Sensorilimbic Connections and Emotion
4.2 Parallel Sensory Pathways to Amygdala: Unique Roles in Emotional Processing
4.3 Neurotransmission and Modulation in Affective Processing Pathways
5 Neural Systems Governing Emotional Expression
5.1 Expression of Emotional Behavior
5.2 Expression of Autonomic Changes Associated With Emotional Behavior
5.3 Emotional Expression: Conclusions
6 Mechanisms of Emotional Experience
7 Brain Mechanisms of Emotion: Conclusions
Figure 1. Figure 1.

Cerebral localization of emotional behavior. Lesion strategies used by early investigators to identify brain areas necessary for expression of emotional behavior are illustrated on midsagittal diagram of cat brain. Transection of midbrain through plane a abolishes integrated emotional responses, allowing expression of only isolated components of emotional behavior. In contrast, emotional behavior survives removal of cerebral cortex (tissue rostral to plane b). Such observations suggested to Cannon 43 and Bard 16 that brain areas below cortex but above midbrain mediate emotional behavior. AC, anterior commissure; CC, corpus callosum; H, hypothalamus; IC, inferior colliculus; OB, olfactory bulb; OC, optic chiasm; S, septum; SC, superior colliculus; T, thalamus.

Adapted from Cannon 43 and Kaada 150
Figure 2. Figure 2.

Papez circuit. Papez proposed that connections between hypothalamus, anterior thalamic nucleus, cingulate gyrus, and hippocampus formed essential emotional network of brain. Sensory input could enter circuit via projections through dorsal thalamus to neocortex and through subcortical projections from ventral thalamus to hypothalamus.

Adapted from Papez 244
Figure 3. Figure 3.

Visceral brain. MacLean 196 described neural substrates of emotion as “visceral brain,” a group of phylogenetically old structures centered around hippocampus. He suggested that correlation of inputs from exteroceptive and interoceptive sensory modalities by hippocampus gives rise to conscious emotional experiences, whereas discharge of hippocampus through hypothalamus accounts for expression of emotional behavior and associated visceral responses. MacLean later introduced the term “limbic system” to refer to this central emotional network.

From MacLean 196, reprinted by permission of Elsevier Science Publishing Co., Inc. Copyright 1949 by The American Psychosomatic Society, Inc
Figure 4. Figure 4.

Limbic lobe. Midsagittal section through human (A) and monkey (B) brain illustrating cortical regions of limbic lobe (hatched area).

From Damasio and Van Hoesen 61
Figure 5. Figure 5.

Dorsomedial and basolateral divisions of limbic forebrain. Dorsomedial division (A) is centered around hippocampus, whereas amygdala is focal point of basolateral division (B).

From Livingston and Escobar 187. Copyright 1971, American Medical Association
Figure 6. Figure 6.

Connections between sensory cortex and limbic forebrain. Sensory inputs are relayed through thalamus to primary receiving areas (koniocortices). Koniocortices project locally to unimodal association areas, which in turn project to areas in which sensory input converges (polymodal association zones) and to limbic forebrain. Polymodal cortex projects to complex (supramodal) association cortex and to limbic areas. Limbic areas also receive inputs from supramodal cortex and some limbic areas (rhinal cortices and hippocampus) qualify as supramodal cortex.

Based on Jones and Powell 147, Mesulam et al. 211, and Swanson 317
Figure 7. Figure 7.

Projections from acoustic thalamus to subcortical forebrain. Cells in areas of rat acoustic thalamus [projection field of inferior colliculus (A)] give rise to fibers terminating in several regions of subcortical forebrain (B), including amygdala, posterior caudate nucleus‐putamen, and hypothalamus. ACE, central nucleus of amygdala; AL, lateral nucleus of amygdala; CI, internal capsule; CPU, caudate nucleus‐putamen; IC, inferior colliculus; MGD, MGM, MGV, dorsal, medial, and ventral divisions of medial geniculate body; MZ, marginal zone; PIN, posterior intralaminar nucleus; PL, posterior limitans nucleus; PP, peripeduncular region; SG, suprageniculate nucleus; SPFL, lateral component of subparafascicular nucleus; VMH, ventromedial nucleus of hypothalamus.

Adapted from LeDoux et al. 180
Figure 8. Figure 8.

Unit activity in amygdala during stimulus evaluation. Top: at end of tone warning signal, a shutter opened to show monkey syringe filled with fruit juice (rewarding) or saline (aversive). Although amygdala cell being recorded from responded to both stimuli, response was greater to rewarding stimulus. Bottom: peristimulus histograms for cell on 10 rewarding and 10 saline trials (bin width, 10 ms).

From Sanghera et al. 290
Figure 9. Figure 9.

Lesions of subcortical, but not cortical, auditory processing areas disrupt conditioning of emotional responses to acoustic stimuli. A: conditioned emotional response in rat consists of increases in mean arterial pressure (MAP) and suppression of locomotor activity (freezing) in presence of tone previously paired with foot shock. MAP response is measured during 10‐s presentation of tone and freezing response during 120‐s presentation. Bilateral destruction of medial geniculate body (MG) or inferior colliculus (IC) disrupted conditioning of emotional responses, whereas ablation of auditory cortex bilaterally had no effect. These data suggest that emotional conditioning depends on relay of acoustic signals through IC to MG and from there to target other than auditory cortex. Critical projection from MG involves amygdala (see Fig. 10). B: representative lesions of auditory cortex (left), MG (center), and IC (right). CG, central gray; CP, cerebral peduncle; IC, inferior colliculus; LL, lateral lemniscus; MG, medial geniculate body; ML, medial lemniscus; PP, peripeduncular region; RN, red nucleus; SC, superior colliculus; SN, substantia nigra.

Adapted from LeDoux et al. 183
Figure 10. Figure 10.

Neural pathway mediating fear conditioning. Conditioning of autonomic and behavioral emotional responses to acoustic stimuli in rat is mediated by sensory signals ascending in primary auditory pathway through IC to MG and then relayed to subcortical region involving dorsal aspects of amygdala, including lateral and central nuclei and fundus striati. In amygdala, pathways mediating autonomic and behavioral responses diverge. Autonomic changes involve connections between dorsal amygdala and lateral hypothalamus (see Fig. 14), and projections from amygdala to or through midbrain mediate behavioral responses (not illustrated). Although auditory pathways decussate in the brain stem, they are illustrated as a homolateral projection here for convenience. ABL, basolateral amygdala; ABM, basomedial amygdala; ACE, central amygdala; AL, lateral amygdala; AM, medial amygdala; CG, central gray; CP, cerebral peduncle; CPU, caudate nucleus‐putamen; CS, conditioned stimulus; F, fornix; FST, fundus striati; IC, inferior colliculus; LH, lateral hypothalamus; MG, medial geniculate body; MRF, midbrain reticular formation; OT, optic tract; PP, peripeduncular region; SN, substantia nigra; ST, stria terminalis; THAL, thalamus; VMH, ventromedial hypothalamus.

Data from LeDoux et al. 183 and Iwata et al. 140,141
Figure 11. Figure 11.

Sensory projections to amygdala and emotional evaluation. Amygdala receives inputs from various exteroceptive and interoceptive sensory modalities (dashed lines). Density of dashed input lines to amygdala signifies extent to which sensory signal is processed before reaching amygdala. Inputs arriving from various cortical association fields have been transformed more than inputs arriving directly from thalamus or nucleus tractus solitarii (NTS). Different inputs may mediate unique aspects of emotional processing, each capable of initiating changes in emotional behavior and autonomic and humoral activity.
Figure 12. Figure 12.

Forms of aggressive behavior. A: affective attack, characterized by emotional display (hissing, baring of teeth) and autonomic reactivity (piloerection, changes in blood pressure), elicited by electrical stimulation of ventromedial region of hypothalamus. B: predatory attack, behavior pattern associated with food acquisition and consumption, elicited by electrical stimulation of lateral areas of hypothalamus.

From Flynn 92
Figure 13. Figure 13.

Contribution of norepinephrine to defensive behavior. Changes in monoaminergic transmitter concentration in brain stem and adrenal gland during rage behavior produced by amygdala stimulation. DA, dopamine; E, epinephrine; NE, norepinephrine; ns, not significant.

From Reis 264
Figure 14. Figure 14.

Destruction of intrinsic neurons in lateral hypothalamus disrupts autonomic but not behavioral components of conditioned fear. A: polygraph tracings illustrating arterial pressure response elicited by acoustic conditioned stimulus (CS) previously paired with foot shock in normal rats and rats receiving bilateral injections of ibotenic acid in lateral (LH) or medial (MH) hypothalamus. B: quantitative, computer‐assisted reconstruction of conditioned pressor response. Pressor response in LH group is significantly smaller than in normal and MH groups. LH lesions reduced pressor response to level seen in unoperated rats given nonassociative (pseudoconditioned) presentations of CS and foot shock. C: neither LH nor MH lesions affected conditioned emotional behavior (freezing). D: typical area of cell loss (hatched areas) produced by injection of ibotenic acid into lateral hypothalamus. E: cell loss in medial hypothalamus produced by ibotenic acid injection. F: location of labeled neurons in hypothalamus after injection of retrograde axonal marker into spinal cord. Various findings suggest spinal projecting neurons in lateral hypothalamus mediate autonomic but not behavioral responses associated with conditioned fear. Afferent connections mediating fear conditioning involve projections from medial geniculate body to amygdala (see Fig. 10). Values illustrated (B, C) represent mean ± SE.

From Iwata et al. 140
Figure 15. Figure 15.

Amygdala central nucleus and conditioned bradycardia in rabbit. A: mean percentage of change in heart rate to 5‐s acoustic conditioned stimulus (CS) relative to pre‐CS base‐line period during aversive classical conditioning. Each group consisted of 8 subjects. Data points represent group means for 15 trial blocks. Large ace, group with bilateral lesions damaging >50% of amygdala central nucleus; small ace, group sustaining bilateral lesions damaging <50% of central amygdala; unop cond, unoperated control group; surg cond, surgical control group; unop pseudo, unoperated control group receiving random, unpaired presentations of CS and eye shock. B: heart rate response produced by medial central nucleus stimulation in awake, loosely restrained rabbit. Upper trace depicts stimulation period, a 1.0‐s stimulus train (40 μA, 100 Hz, 0.5 ms). Lower trace is cardiotachograph response. C: thionin‐stained frontal section of rabbit brain showing recording electrode tract coursing through amygdala central nucleus. At conclusion of recording session small marker lesions were made at 1‐mm intervals. Arrow depicts region in which neurons of type shown in D were located. ACE, amygdala central nucleus; Bl, basolateral nucleus; Bm, basomedial nucleus; La, lateral nucleus; Me, medial nucleus; OT, optic tract. D : oscilloscope traces show responses of an amygdala central nucleus neuron to presentation of tone (CS+) paired with shock, and second tone (CS‐) never paired with shock during differential classical conditioning. A 5.0‐s pre‐CS base‐line period begins on left. Onset of each 5.0‐s CS is indicated by dashed vertical line. Calibration bar = 1.0 s. Note preferentially increased activity to CS+. In neurons of this type, magnitudes of neuronal responses to CS+ often were correlated with magnitudes of concomitant bradycardic response.

Adapted from Kapp et al. 152 and Pascoe and Kapp 245
Figure 16. Figure 16.

Interhemispheric attribution. Tests involving split‐brain patient in whom either hemisphere could read and execute simple motor commands, but only left could speak. Commands were presented to left visual field, and thus to the right hemisphere, as patient fixated on spot in center of screen. In each instance right hemisphere correctly performs commanded action. Left hemisphere has not seen command and thus does not really know why behavior was performed but readily offers explanations as if it knows. Such explanations are based on observations of overt behavior performed by right hemisphere.

From Gazzaniga and LeDoux 103
Figure 17. Figure 17.

Limbic seizures. Seizure activity starting in right hippocampus (RB1) and involving right amygdala (RA1) and right parahippocampal gyrus (RC1). Seizure remains largely in limbic areas. Neocortical areas (RC3–5, RFS1–5) are minimally involved. Seizure ultimately becomes bilateral. Note experiential phenomena associated with seizure.

From Gloor et al. 107


Figure 1.

Cerebral localization of emotional behavior. Lesion strategies used by early investigators to identify brain areas necessary for expression of emotional behavior are illustrated on midsagittal diagram of cat brain. Transection of midbrain through plane a abolishes integrated emotional responses, allowing expression of only isolated components of emotional behavior. In contrast, emotional behavior survives removal of cerebral cortex (tissue rostral to plane b). Such observations suggested to Cannon 43 and Bard 16 that brain areas below cortex but above midbrain mediate emotional behavior. AC, anterior commissure; CC, corpus callosum; H, hypothalamus; IC, inferior colliculus; OB, olfactory bulb; OC, optic chiasm; S, septum; SC, superior colliculus; T, thalamus.

Adapted from Cannon 43 and Kaada 150


Figure 2.

Papez circuit. Papez proposed that connections between hypothalamus, anterior thalamic nucleus, cingulate gyrus, and hippocampus formed essential emotional network of brain. Sensory input could enter circuit via projections through dorsal thalamus to neocortex and through subcortical projections from ventral thalamus to hypothalamus.

Adapted from Papez 244


Figure 3.

Visceral brain. MacLean 196 described neural substrates of emotion as “visceral brain,” a group of phylogenetically old structures centered around hippocampus. He suggested that correlation of inputs from exteroceptive and interoceptive sensory modalities by hippocampus gives rise to conscious emotional experiences, whereas discharge of hippocampus through hypothalamus accounts for expression of emotional behavior and associated visceral responses. MacLean later introduced the term “limbic system” to refer to this central emotional network.

From MacLean 196, reprinted by permission of Elsevier Science Publishing Co., Inc. Copyright 1949 by The American Psychosomatic Society, Inc


Figure 4.

Limbic lobe. Midsagittal section through human (A) and monkey (B) brain illustrating cortical regions of limbic lobe (hatched area).

From Damasio and Van Hoesen 61


Figure 5.

Dorsomedial and basolateral divisions of limbic forebrain. Dorsomedial division (A) is centered around hippocampus, whereas amygdala is focal point of basolateral division (B).

From Livingston and Escobar 187. Copyright 1971, American Medical Association


Figure 6.

Connections between sensory cortex and limbic forebrain. Sensory inputs are relayed through thalamus to primary receiving areas (koniocortices). Koniocortices project locally to unimodal association areas, which in turn project to areas in which sensory input converges (polymodal association zones) and to limbic forebrain. Polymodal cortex projects to complex (supramodal) association cortex and to limbic areas. Limbic areas also receive inputs from supramodal cortex and some limbic areas (rhinal cortices and hippocampus) qualify as supramodal cortex.

Based on Jones and Powell 147, Mesulam et al. 211, and Swanson 317


Figure 7.

Projections from acoustic thalamus to subcortical forebrain. Cells in areas of rat acoustic thalamus [projection field of inferior colliculus (A)] give rise to fibers terminating in several regions of subcortical forebrain (B), including amygdala, posterior caudate nucleus‐putamen, and hypothalamus. ACE, central nucleus of amygdala; AL, lateral nucleus of amygdala; CI, internal capsule; CPU, caudate nucleus‐putamen; IC, inferior colliculus; MGD, MGM, MGV, dorsal, medial, and ventral divisions of medial geniculate body; MZ, marginal zone; PIN, posterior intralaminar nucleus; PL, posterior limitans nucleus; PP, peripeduncular region; SG, suprageniculate nucleus; SPFL, lateral component of subparafascicular nucleus; VMH, ventromedial nucleus of hypothalamus.

Adapted from LeDoux et al. 180


Figure 8.

Unit activity in amygdala during stimulus evaluation. Top: at end of tone warning signal, a shutter opened to show monkey syringe filled with fruit juice (rewarding) or saline (aversive). Although amygdala cell being recorded from responded to both stimuli, response was greater to rewarding stimulus. Bottom: peristimulus histograms for cell on 10 rewarding and 10 saline trials (bin width, 10 ms).

From Sanghera et al. 290


Figure 9.

Lesions of subcortical, but not cortical, auditory processing areas disrupt conditioning of emotional responses to acoustic stimuli. A: conditioned emotional response in rat consists of increases in mean arterial pressure (MAP) and suppression of locomotor activity (freezing) in presence of tone previously paired with foot shock. MAP response is measured during 10‐s presentation of tone and freezing response during 120‐s presentation. Bilateral destruction of medial geniculate body (MG) or inferior colliculus (IC) disrupted conditioning of emotional responses, whereas ablation of auditory cortex bilaterally had no effect. These data suggest that emotional conditioning depends on relay of acoustic signals through IC to MG and from there to target other than auditory cortex. Critical projection from MG involves amygdala (see Fig. 10). B: representative lesions of auditory cortex (left), MG (center), and IC (right). CG, central gray; CP, cerebral peduncle; IC, inferior colliculus; LL, lateral lemniscus; MG, medial geniculate body; ML, medial lemniscus; PP, peripeduncular region; RN, red nucleus; SC, superior colliculus; SN, substantia nigra.

Adapted from LeDoux et al. 183


Figure 10.

Neural pathway mediating fear conditioning. Conditioning of autonomic and behavioral emotional responses to acoustic stimuli in rat is mediated by sensory signals ascending in primary auditory pathway through IC to MG and then relayed to subcortical region involving dorsal aspects of amygdala, including lateral and central nuclei and fundus striati. In amygdala, pathways mediating autonomic and behavioral responses diverge. Autonomic changes involve connections between dorsal amygdala and lateral hypothalamus (see Fig. 14), and projections from amygdala to or through midbrain mediate behavioral responses (not illustrated). Although auditory pathways decussate in the brain stem, they are illustrated as a homolateral projection here for convenience. ABL, basolateral amygdala; ABM, basomedial amygdala; ACE, central amygdala; AL, lateral amygdala; AM, medial amygdala; CG, central gray; CP, cerebral peduncle; CPU, caudate nucleus‐putamen; CS, conditioned stimulus; F, fornix; FST, fundus striati; IC, inferior colliculus; LH, lateral hypothalamus; MG, medial geniculate body; MRF, midbrain reticular formation; OT, optic tract; PP, peripeduncular region; SN, substantia nigra; ST, stria terminalis; THAL, thalamus; VMH, ventromedial hypothalamus.

Data from LeDoux et al. 183 and Iwata et al. 140,141


Figure 11.

Sensory projections to amygdala and emotional evaluation. Amygdala receives inputs from various exteroceptive and interoceptive sensory modalities (dashed lines). Density of dashed input lines to amygdala signifies extent to which sensory signal is processed before reaching amygdala. Inputs arriving from various cortical association fields have been transformed more than inputs arriving directly from thalamus or nucleus tractus solitarii (NTS). Different inputs may mediate unique aspects of emotional processing, each capable of initiating changes in emotional behavior and autonomic and humoral activity.



Figure 12.

Forms of aggressive behavior. A: affective attack, characterized by emotional display (hissing, baring of teeth) and autonomic reactivity (piloerection, changes in blood pressure), elicited by electrical stimulation of ventromedial region of hypothalamus. B: predatory attack, behavior pattern associated with food acquisition and consumption, elicited by electrical stimulation of lateral areas of hypothalamus.

From Flynn 92


Figure 13.

Contribution of norepinephrine to defensive behavior. Changes in monoaminergic transmitter concentration in brain stem and adrenal gland during rage behavior produced by amygdala stimulation. DA, dopamine; E, epinephrine; NE, norepinephrine; ns, not significant.

From Reis 264


Figure 14.

Destruction of intrinsic neurons in lateral hypothalamus disrupts autonomic but not behavioral components of conditioned fear. A: polygraph tracings illustrating arterial pressure response elicited by acoustic conditioned stimulus (CS) previously paired with foot shock in normal rats and rats receiving bilateral injections of ibotenic acid in lateral (LH) or medial (MH) hypothalamus. B: quantitative, computer‐assisted reconstruction of conditioned pressor response. Pressor response in LH group is significantly smaller than in normal and MH groups. LH lesions reduced pressor response to level seen in unoperated rats given nonassociative (pseudoconditioned) presentations of CS and foot shock. C: neither LH nor MH lesions affected conditioned emotional behavior (freezing). D: typical area of cell loss (hatched areas) produced by injection of ibotenic acid into lateral hypothalamus. E: cell loss in medial hypothalamus produced by ibotenic acid injection. F: location of labeled neurons in hypothalamus after injection of retrograde axonal marker into spinal cord. Various findings suggest spinal projecting neurons in lateral hypothalamus mediate autonomic but not behavioral responses associated with conditioned fear. Afferent connections mediating fear conditioning involve projections from medial geniculate body to amygdala (see Fig. 10). Values illustrated (B, C) represent mean ± SE.

From Iwata et al. 140


Figure 15.

Amygdala central nucleus and conditioned bradycardia in rabbit. A: mean percentage of change in heart rate to 5‐s acoustic conditioned stimulus (CS) relative to pre‐CS base‐line period during aversive classical conditioning. Each group consisted of 8 subjects. Data points represent group means for 15 trial blocks. Large ace, group with bilateral lesions damaging >50% of amygdala central nucleus; small ace, group sustaining bilateral lesions damaging <50% of central amygdala; unop cond, unoperated control group; surg cond, surgical control group; unop pseudo, unoperated control group receiving random, unpaired presentations of CS and eye shock. B: heart rate response produced by medial central nucleus stimulation in awake, loosely restrained rabbit. Upper trace depicts stimulation period, a 1.0‐s stimulus train (40 μA, 100 Hz, 0.5 ms). Lower trace is cardiotachograph response. C: thionin‐stained frontal section of rabbit brain showing recording electrode tract coursing through amygdala central nucleus. At conclusion of recording session small marker lesions were made at 1‐mm intervals. Arrow depicts region in which neurons of type shown in D were located. ACE, amygdala central nucleus; Bl, basolateral nucleus; Bm, basomedial nucleus; La, lateral nucleus; Me, medial nucleus; OT, optic tract. D : oscilloscope traces show responses of an amygdala central nucleus neuron to presentation of tone (CS+) paired with shock, and second tone (CS‐) never paired with shock during differential classical conditioning. A 5.0‐s pre‐CS base‐line period begins on left. Onset of each 5.0‐s CS is indicated by dashed vertical line. Calibration bar = 1.0 s. Note preferentially increased activity to CS+. In neurons of this type, magnitudes of neuronal responses to CS+ often were correlated with magnitudes of concomitant bradycardic response.

Adapted from Kapp et al. 152 and Pascoe and Kapp 245


Figure 16.

Interhemispheric attribution. Tests involving split‐brain patient in whom either hemisphere could read and execute simple motor commands, but only left could speak. Commands were presented to left visual field, and thus to the right hemisphere, as patient fixated on spot in center of screen. In each instance right hemisphere correctly performs commanded action. Left hemisphere has not seen command and thus does not really know why behavior was performed but readily offers explanations as if it knows. Such explanations are based on observations of overt behavior performed by right hemisphere.

From Gazzaniga and LeDoux 103


Figure 17.

Limbic seizures. Seizure activity starting in right hippocampus (RB1) and involving right amygdala (RA1) and right parahippocampal gyrus (RC1). Seizure remains largely in limbic areas. Neocortical areas (RC3–5, RFS1–5) are minimally involved. Seizure ultimately becomes bilateral. Note experiential phenomena associated with seizure.

From Gloor et al. 107
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Article Title: Emotion
 

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Joseph E. LeDoux. Emotion. Compr Physiol 2011, Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain: 419-459. First published in print 1987. doi: 10.1002/cphy.cp010510