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Social network size has been associated with complex socio-cognitive processes (e.g., memory, perspective taking). Supporting this idea, recent neuroimaging studies in healthy adults have reported a relationship between social network size and brain volumes in regions related to memory and social cognition (e.g., hippocampus, amygdala). Lesion-deficit studies in neurological patients are rare and have been inconclusive due to differences in participant sampling and measurement. The present study uses a multiple case study approach. We investigated patients with focal damage to the hippocampus and/or amygdala (two neural structures thought to be critical for social networks), and examined the patients' social network size, loneliness, and life satisfaction relative to a non-injured comparison group. Patients with amygdalar damage had smaller social networks and reported higher levels of loneliness and lower life satisfaction, on average, than comparison participants. Patients with damage to the hippocampus reported more friends than the comparison participants, but did not differ in their ratings of loneliness or life satisfaction. This lesion study offers new evidence that the amygdala is critical for social networks, life satisfaction, and reduced loneliness., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

The amygdala is a subcortical structure implicated in both the expression of conditioned fear and social fear recognition. Social fear recognition deficits following amygdala lesions are often interpreted as reflecting perceptual deficits, or the amygdala's role in coordinating responses to threats. But these explanations fail to capture why amygdala lesions impair both physiological and behavioural responses to multimodal fear cues and the ability to identify them. We hypothesized that social fear recognition deficits following amygdala damage reflect impaired conceptual understanding of fear. Supporting this prediction, we found specific impairments in the ability to predict others' fear (but not other emotions) from written scenarios following bilateral amygdala lesions. This finding is consistent with the suggestion that social fear recognition, much like social recognition of states like pain, relies on shared internal representations. Preserved judgements about the permissibility of causing others fear confirms suggestions that social emotion recognition and morality are dissociable.

BACKGROUNDSeizure-induced inhibition of respiration plays a critical role in sudden unexpected death in epilepsy (SUDEP). However, the mechanisms underlying seizure-induced central apnea in pediatric epilepsy are unknown.METHODSWe studied 8 pediatric patients with intractable epilepsy undergoing intracranial electroencephalography. We recorded respiration during seizures and during electrical stimulation mapping of 174 forebrain sites. A machine-learning algorithm was used to delineate brain regions that inhibit respiration.RESULTSIn 2 patients, apnea coincided with seizure spread to the amygdala. Supporting a role for the amygdala in breathing inhibition in children, electrically stimulating the amygdala produced apnea in all 8 subjects (3-17 years old). These effects did not depend on epilepsy type and were relatively specific to the amygdala, as no other site affected breathing. Remarkably, patients were unaware that they had stopped breathing, and none reported dyspnea or arousal, findings critical for SUDEP. Finally, a machine-learning algorithm based on 45 stimulation sites and 210 stimulation trials identified a focal subregion in the human amygdala that consistently produced apnea. This site, which we refer to as the amygdala inhibition of respiration (AIR) site includes the medial subregion of the basal nuclei, cortical and medial nuclei, amygdala transition areas, and intercalated neurons.CONCLUSIONSA focal site in the amygdala inhibits respiration and induces apnea (AIR site) when electrically stimulated and during seizures in children with epilepsy. This site may prove valuable for determining those at greatest risk for SUDEP and as a therapeutic target.FUNDINGNational Institute of Neurological Disorders and Stroke - Congress of Neurological Surgeons, National Institute of General Medical Sciences, Roy J. Carver Charitable Trust.

The fearlessness model posits that psychopathy is underpinned by a deficiency in the capacity to experience fear, predisposing to other features of the condition, such as superficial charm, guiltlessness, callousness, narcissism, and dishonesty. Nevertheless, it is unclear whether fearlessness is irrelevant, necessary, sufficient, or merely contributory to psychopathy. In the present case study, we sought to examine the fearlessness model by studying an extensively investigated female patient-S. M.-who experienced early emerging bilateral calcifications of the amygdala, resulting in a virtual absence of fear. We aimed to replicate findings regarding S. M.'s deficient experience of self-reported fear and examine her levels of triarchic psychopathy dimensions (boldness, meanness, disinhibition). We also examined S. M.'s history of heroic behaviors given conjectures that fearlessness contributes to both heroism and psychopathy. Compared with population-based norms, S. M. reported deficient levels of self-reported fear and self-control, as well as elevated levels of heroism. She did not, however, exhibit elevated levels of the core affective deficits of psychopathy, as reflected in measures of coldheartedness and meanness. These findings suggest that severe fear deficits may be insufficient to yield the full clinical picture of psychopathy, although they do not preclude the possibility that these deficits are necessary. (PsycINFO Database Record, ((c) 2018 APA, all rights reserved).)

A growing body of literature demonstrates that racial group membership can influence neural responses, e.g. when individuals perceive or interact with persons of another race. However, little attention has been paid to social class, a factor that interacts with racial inequalities in American society. We extend previous literature on race-related neural activity by focusing on how the human brain responds to racial out-groups cast in positively valued social class positions vs less valued ones. We predicted that the ventromedial prefrontal cortex (vmPFC) and the amygdala would have functionally dissociable roles, with the vmPFC playing a more significant role within socially valued in-groups (i.e. the middle-class) and the amygdala having a more crucial role for socially ambivalent and threatening categories (i.e. upper and lower class). We tested these predictions with two complementary studies: (i) a neuropsychological experiment with patients with the vmPFC or amygdala lesions, contrasted with brain damaged and normal comparison participants, and (ii) a functional magnetic resonance imaging experiment with 15 healthy adults. Our findings suggest that two distinct mechanisms underlie class-based racial evaluations, one engaging the vmPFC for positively identified in-group class and another recruiting the amygdala for the class groups that are marginalized or perceived as potential threats., (© The Author (2017). Published by Oxford University Press.)

The amygdala and the hippocampus are associated with emotional processing and declarative memory, respectively. Studies have shown that patients with bilateral hippocampal damage caused by anoxia/ischemia, and patients with probable Alzheimer's disease (AD), can experience emotions for prolonged periods of time, even when they cannot remember what caused the emotion in the first place (Feinstein et al. (2010) Proc Natl Acad Sci USA 107:7674-7679; Guzmán-Vélez et al. (2014) Cogn Behav Neurol 27:117-129). This study aimed to investigate, for the first time, the roles of the amygdala and hippocampus in the dissociation between feelings of emotion and declarative memory for emotion-inducing events in patients with AD. Individuals with probable AD (N = 12) and age-matched healthy comparisons participants (HCP; N = 12) completed a high-resolution (0.44 × 0.44 × 0.80 mm) T2-weighted structural MR scan of the medial temporal lobe. Each of these individuals also completed two separate emotion induction procedures (sadness and happiness) using film clips. We collected real-time emotion ratings at baseline and multiple times postinduction, and administered a test of declarative memory shortly after each induction. Consistent with previous research, hippocampal volume was significantly smaller in patients with AD compared with HCP, and was positively correlated with memory for the film clips. Sustained feelings of emotion and amygdala volume did not significantly differ between patients with AD and HCP. Follow-up analyses showed a significant negative correlation between amygdala volume and sustained sadness, and a significant positive correlation between amygdala volume and sustained happiness. Our findings suggest that the amygdala is important for regulating and sustaining an emotion independent of hippocampal function and declarative memory for the emotion-inducing event. © 2015 Wiley Periodicals, Inc., (© 2015 Wiley Periodicals, Inc.)

Functional neuroimaging investigations of pain have discovered a reliable pattern of activation within limbic regions of a putative "pain matrix" that has been theorized to reflect the affective dimension of pain. To test this theory, we evaluated the experience of pain in a rare neurological patient with extensive bilateral lesions encompassing core limbic structures of the pain matrix, including the insula, anterior cingulate, and amygdala. Despite widespread damage to these regions, the patient's expression and experience of pain was intact, and at times excessive in nature. This finding was consistent across multiple pain measures including self-report, facial expression, vocalization, withdrawal reaction, and autonomic response. These results challenge the notion of a "pain matrix" and provide direct evidence that the insula, anterior cingulate, and amygdala are not necessary for feeling the suffering inherent to pain. The patient's heightened degree of pain affect further suggests that these regions may be more important for the regulation of pain rather than providing the decisive substrate for pain's conscious experience.

Decades of research have highlighted the amygdala's influential role in fear. We found that inhalation of 35% CO(2) evoked not only fear, but also panic attacks, in three rare patients with bilateral amygdala damage. These results indicate that the amygdala is not required for fear and panic, and make an important distinction between fear triggered by external threats from the environment versus fear triggered internally by CO(2).

The human amygdalae are involved in processing visual information about the eyes within faces, and play an essential role in the use of information from the eye region of the face in order to judge emotional expressions, as well as in directing gaze to the eyes in conversations with real people. However, the roles played here by the left and right amygdala individually remain unknown. Here we investigated this question by applying the 'Bubbles' method, which asks viewers to discriminate facial emotions from randomly sampled small regions of a face, to 23 neurological participants with focal, unilateral amygdala damage (10 to the right amygdala). We found a statistically significant asymmetry in the use of eye information when comparing those with unilateral left lesions to those with unilateral right lesions, specifically during emotion judgments. The findings have implications for the amygdala's role in emotion recognition and gaze direction during face processing.

Decision-making is a complex process that requires the orchestration of multiple neural systems. For example, decision-making is believed to involve areas of the brain involved in emotion (e.g., amygdala, ventromedial prefrontal cortex) and memory (e.g., hippocampus, dorsolateral prefrontal cortex). In this article, we will present findings related to the amygdala's role in decision-making, and differentiate the contributions of the amygdala from those of other structurally and functionally connected neural regions. Decades of research have shown that the amygdala is involved in associating a stimulus with its emotional value. This tradition has been extended in newer work, which has shown that the amygdala is especially important for decision-making, by triggering autonomic responses to emotional stimuli, including monetary reward and punishment. Patients with amygdala damage lack these autonomic responses to reward and punishment, and consequently, cannot utilize "somatic marker" type cues to guide future decision-making. Studies using laboratory decision-making tests have found deficient decision-making in patients with bilateral amygdala damage, which resembles their real-world difficulties with decision-making. Additionally, we have found evidence for an interaction between sex and laterality of amygdala functioning, such that unilateral damage to the right amygdala results in greater deficits in decision-making and social behavior in men, while left amygdala damage seems to be more detrimental for women. We have posited that the amygdala is part of an "impulsive," habit type system that triggers emotional responses to immediate outcomes., (Copyright © 2010 Elsevier Ltd. All rights reserved.)

The human amygdala is known to be involved in processing social, emotional, and reward-related information. Previous reports have indicated that the amygdala is involved in extracting trustworthiness information from faces. Interestingly, functional neuroimaging research using economic tasks that presumably require developing and/or expressing interpersonal trust, such as the Trust Game (TG), have not routinely identified involvement of the amygdala. The present study sought to explore the role of the amygdala in developing and expressing interpersonal trust, via a multi-round, multiplayer economic exchange, a version of the TG, in a large sample of participants with focal brain damage. Participants with unilateral damage to the amygdala displayed increased benevolent behavior in the TG, and specifically, they tended to increase trust in response to betrayals. On the other hand, neurologically normal adults tended to repay trust in kind, i.e., they decreased interpersonal trust in response to betrayals or increased trust in response to increases from others. Comparison participants, with brain damage that does not include the amygdala, ventromedial prefrontal or insular cortices, tended to behave ambivalently to the expressed trust or betrayal of others. Our data suggest that the amygdala is necessary for developing and expressing normal interpersonal trust. This increased tendency to behave benevolently in response to defections from others may be related to the abnormal social behavior observed in this group. Moreover, increased benevolence may increase the likelihood or opportunity to be taken advantage of by others., (Copyright © 2010 Elsevier Ltd. All rights reserved.)

Objective: The development of "common ground," or mutual knowledge of shared information, is believed to require the ability to update a mental representation of another person's thoughts and knowledge based on verbal information and nonverbal social and emotional signals, to facilitate economical communication. As in other forms of everyday social communication, the development of common ground likely requires the orchestration of multiple cognitive processes supported by various neural systems. Here, we investigate the contribution of the amygdala to these processes., Method: SM, a patient with complete, focal, bilateral amygdala damage, and deficits in social and emotional processing, and five healthy comparison participants, each interacted with a familiar partner. We investigated the participants' ability to develop and use referential labels across 24 dynamic, collaborative interactions. Participants verbally directed their partner how to arrange a set of 12 abstract tangrams while separated by a low barrier, allowing them to see each other but hiding their tangrams., Results: In contrast to comparison participants, SM exhibited an impaired rate of learning across trials and did not show the typical simplification in the labels generated during the interactions. Detailed analyses of SM's interactional discourse and social behavior suggested that she has impaired perspective-taking or what can be interpreted as deficient "theory of mind," manifested in abnormal "language-in-use.", Conclusions: These results support the conclusion that the amygdala, a structure critical for social and emotional processing, plays an important role in the acquisition and use of common ground and in social communication more broadly.

Although clinical observations suggest that humans with amygdala damage have abnormal fear reactions and a reduced experience of fear, these impressions have not been systematically investigated. To address this gap, we conducted a new study in a rare human patient, SM, who has focal bilateral amygdala lesions. To provoke fear in SM, we exposed her to live snakes and spiders, took her on a tour of a haunted house, and showed her emotionally evocative films. On no occasion did SM exhibit fear, and she never endorsed feeling more than minimal levels of fear. Likewise, across a large battery of self-report questionnaires, 3 months of real-life experience sampling, and a life history replete with traumatic events, SM repeatedly demonstrated an absence of overt fear manifestations and an overall impoverished experience of fear. Despite her lack of fear, SM is able to exhibit other basic emotions and experience the respective feelings. The findings support the conclusion that the human amygdala plays a pivotal role in triggering a state of fear and that the absence of such a state precludes the experience of fear itself., (Copyright © 2011 Elsevier Ltd. All rights reserved.)

Research into the neural underpinnings of fear and fear-related pathology has highlighted the role of the amygdala. For instance, bilateral damage to the amygdaloid complex is associated with decreased appreciation of danger and recognition of fear in humans, whereas enlarged amygdala volume is associated with internalizing syndromes. It is unknown whether amygdala volume and fearfulness are related in the absence of pathology. We examined the correlation between normal fearfulness and amygdala morphology in 116 healthy children and adolescents (60 boys, 56 girls, age 7-17 years). Fearfulness was measured using the parent ratings on the Pediatric Behavior Scale and amygdala volumes were determined by manual tracing. We found a positive correlation between right amygdala volume in girls (r = 0.29). This relationship was more robust and present bilaterally when analyses were limited to girls with a positive nuclear family history of depression (for left r = 0.63; for right r = 0.58). In boys there was no significant relationship which may suggest that biological mechanisms differ between sexes. Given the role of enlarged amygdala volume in pathology, these findings may indicate that variation in amygdala morphology marks susceptibility to internalizing disorders.

We have reported previously that there appears to be an intriguing sex-related functional asymmetry of the prefrontal cortices, especially the ventromedial sector, in regard to social conduct, emotional processing, and decision-making, whereby the right-sided sector is important in men but not women and the left-sided sector is important in women but not men. The amygdala is another structure that has been widely implicated in emotion processing and social decision-making, and the question arises as to whether the amygdala, in a manner akin to what has been observed for the prefrontal cortex, might have sex-related functional asymmetry in regard to social and emotional functions. A preliminary test of this question was carried out in the current study, where we used a case-matched lesion approach and contrasted a pair of men cases and a pair of women cases, where in each pair one patient had left amygdala damage and the other had right amygdala damage. We investigated the domains of social conduct, emotional processing and personality, and decision-making. The results provide support for the notion that there is sex-related functional asymmetry of the amygdala in regard to these functions - in the male pair, the patient with right-sided amygdala damage was impaired in these functions, and the patient with left-sided amygdala damage was not, whereas in the female pair, the opposite pattern obtained, with the left-sided woman being impaired and the right-sided woman being unimpaired. These data provide preliminary support for the notion that sex-related functional asymmetry of the amygdala may entail functions such as social conduct, emotional processing, and decision-making, a finding that in turn could reflect (as either a cause or effect) differences in the manner in which men and women apprehend, process, and execute emotion-related information.

The amygdala has been implicated in emotional processes, although the precise nature of the emotional deficits following amygdala lesions remains to be fully elucidated. Cognitive disturbances in the perception, recognition or memory of emotional stimuli have been suggested by some, whereas others have proposed changes in emotional arousal. To address this issue, measures of emotional arousal and valence (positivity and negativity) to a graded series of emotional pictures were obtained from patients with lesions of the amygdala and from a clinical contrast group with lesions that spared this structure. Relative to the contrast group, patients with damage to the amygdala evidenced a complete lack of an arousal gradient across negative stimuli, although they displayed a typical arousal gradient to positive stimuli. These results were not attributable to the inability of amygdala patients to process the hostile or hospitable nature of the stimuli, as the amygdala group accurately recognized and categorized both positive and negative features of the stimuli. The relative lack of emotional arousal to negative stimuli may account for many of the clinical features of amygdala lesions.

It has been well established that the amygdala is critical for processing various aspects of emotion, and in particular, for the perception of negative emotions such as fear. Perhaps the strongest evidence for this conclusion in humans comes from an extensive series of investigations in patient SM, an extremely rare neurological patient who has complete, focal bilateral amygdala damage. One question that has remained unanswered, however, is whether SM has a normal phenomenological experience of emotion, especially negative emotion. To explore this issue, we designed a study in which two experienced clinical psychologists conducted "blind" interviews of SM (the psychologists were not provided any background information regarding SM), with a special emphasis regarding the nature of her emotional experience. Both of them reached the conclusion that SM expressed a normal range of affect and emotion, and neither felt that SM warranted a DSM-IV diagnosis. However, they both noted that SM was remarkably dispassionate when relating highly emotional and traumatic life experiences, and they noted that she did not seem to have a normal sense of distrust and "danger". To the psychologists, SM came across as a "survivor", as being "resilient" and even "heroic" in the way that she had dealt with adversity in her life. In the full light of SM's neurological and neuropsychological profile, however, these observations reflect the fact that SM is missing from the experiences in her life some of the deepest negative emotions, in a manner that parallels her defect in perceiving such emotions in external stimuli. These findings have interesting parallels with recent animal work (cf. Bauman, Lavenex, Mason, Capitanio, & Amaral, 2004a), and they provide valuable insights into the emotional life of an individual with complete bilateral amygdala damage.

Neurobiological studies demonstrate the amygdala's role in emotional memory, and psychological studies suggest a particular pattern: enhanced memory for the gist but not the details of complex stimuli. We hypothesized that these two findings are related. Whereas normal (n = 52) and brain-damaged (n = 22) controls showed the expected enhancement of gist memory when the encoding context was emotional, persons with unilateral damage to the medial temporal lobe including the amygdala (n = 16) did not show this pattern. Furthermore, amygdala volume showed a significant positive correlation with gist memory but not with overall memory. A further study in four subjects with selective medial temporal damage sparing the amygdala, and one with selective damage confined to the amygdala, confirmed the specificity of this effect to the amygdala. The data support a model whereby the amygdala focuses processing resources on gist, possibly accounting for features of traumatic memories and eyewitness testimony in real life.

Ten years ago, we reported that SM, a patient with rare bilateral amygdala damage, showed an intriguing impairment in her ability to recognize fear from facial expressions. Since then, the importance of the amygdala in processing information about facial emotions has been borne out by a number of lesion and functional imaging studies. Yet the mechanism by which amygdala damage compromises fear recognition has not been identified. Returning to patient SM, we now show that her impairment stems from an inability to make normal use of information from the eye region of faces when judging emotions, a defect we trace to a lack of spontaneous fixations on the eyes during free viewing of faces. Although SM fails to look normally at the eye region in all facial expressions, her selective impairment in recognizing fear is explained by the fact that the eyes are the most important feature for identifying this emotion. Notably, SM's recognition of fearful faces became entirely normal when she was instructed explicitly to look at the eyes. This finding provides a mechanism to explain the amygdala's role in fear recognition, and points to new approaches for the possible rehabilitation of patients with defective emotion perception.

Although the amygdala's role in processing facial expressions of fear has been well established, its role in the processing of other emotions is unclear. In particular, evidence for the amygdala's involvement in processing expressions of happiness and sadness remains controversial. To clarify this issue, we constructed a series of morphed stimuli whose emotional expression varied gradually from very faint to more pronounced. Five morphs each of sadness and happiness, as well as neutral faces, were shown to 27 subjects with unilateral amygdala damage and 5 with complete bilateral amygdala damage, whose data were compared to those from 12 brain damaged and 26 normal controls. Subjects were asked to rate the intensity and to label the stimuli. Subjects with unilateral amygdala damage performed very comparably to controls. By contrast, subjects with bilateral amygdala damage showed a specific impairment in rating sad faces, but performed normally in rating happy faces. Furthermore, subjects with right unilateral amygdala damage performed somewhat worse than subjects with left unilateral amygdala damage. The findings suggest that the amygdala's role in processing of emotional facial expressions encompasses multiple negatively valenced emotions, including fear and sadness.

The acoustic startle reflex (ASR) is potentiated during negative emotion, but attenuated during positive emotional experience. The modulation of the ASR by fear depends critically on the amygdala. The authors investigated ASR modulation to fearful, disgusting, pleasant, and neutral stimuli in 12 patients with unilateral damage to the anteromedial temporal lobe including the amygdala (6 left, 6 right), 1 patient with bilateral temporal lobe damage including the amygdala, and 12 comparison participants. Both groups with unilateral damage, as well as the subject with bilateral damage, showed a complete lack of ASR potentiation to both fear and disgust stimuli. The findings suggest that potentiation of the ASR by disgust and fear depends on the integrity of the anteromedial temporal lobe.

The medial temporal lobe is known to play a role in the processing of olfaction and memory. The specific contribution of the human amygdala to memory for odors has not been addressed, however. The role of this region in memory for odors was assessed in patients with unilateral amygdala damage due to temporal lobectomy (n = 20; 11 left, 9 right), one patient with selective bilateral amygdala damage, and in 20 age-matched normal controls. Fifteen odors were presented, followed 1 h later by an odor-name matching test and an odor-odor recognition test. Signal detection analyses showed that both unilateral groups were impaired in their memory for matching odors with names, these patients were not significantly impaired on odor-odor recognition. Bilateral amygdala damage resulted in severe impairment in both odor-name matching as well as in odor-odor recognition memory. Importantly, none of the patients were impaired on an auditory verbal learning task, suggesting that these findings reflect a specific impairment in olfactory memory, and not merely a more general memory deficit. Taken together, the data provide neuropsychological evidence that the human amygdala is essential for olfactory memory.

Bilateral damage to the human amygdala impairs recognition of negatively valenced emotions from facial expressions, but it is unclear if this finding generalizes to richer visual stimuli that contain cues in addition to faces. We investigated this issue in 4 subjects with bilateral amygdala damage, 23 with unilateral amygdala damage, 22 brain-damaged controls and 16 normal individuals. Subjects were shown two blocks of complex social scenes; all stimuli in the two blocks were identical, except that the first block had all facial expressions in the image erased. While control subjects were more accurate in recognizing emotions when facial expressions were present, subjects with bilateral amygdala damage did not show the same benefit for negative emotions, often performing equivalently across the two conditions. Most striking, subjects with bilateral amygdala damage were more accurate in recognizing scenes showing anger with faces erased than with faces present, an effect resulting in part from highly abnormal recognition of certain angry facial expressions. All four subjects with bilateral amygdala damage were impaired in recognizing angry faces shown in isolation, and frequently mistook expressions of anger for smiles, a mistake never made by any control subject. Bilateral amygdala damage thus disproportionately impairs recognition of certain emotions from complex visual stimuli when subjects utilize information from facial expressions.

Lesion, functional imaging, and single-unit studies in human and nonhuman animals have demonstrated a role for the amygdala in processing stimuli with emotional and social significance. We investigated the recognition of a wide variety of facial expressions, including basic emotions (e.g., happiness, anger) and social emotions (e.g., guilt, admiration, flirtatiousness). Prior findings with a standardized set of stimuli indicated that recognition of social emotions can be signaled by the eye region of the face and is disproportionately impaired in autism (Baron-Cohen, Wheelwright, & Jolliffe, 1997). To test the hypothesis that the recognition of social emotions depends on the amygdala, we administered the same stimuli to 30 subjects with unilateral amygdala damage (16 left, 14 right), 2 with bilateral amygdala damage, 47 brain-damaged controls, and 19 normal controls. Compared with controls, subjects with unilateral or bilateral amygdala damage were impaired when recognizing social emotions; moreover, they were more impaired in recognition of social emotions than in recognition of basic emotions, and, like previously described patients with autism, they were impaired also when asked to recognize social emotions from the eye region of the face alone. The findings suggest that the human amygdala is relatively specialized to process stimuli with complex social significance. The results also provide further support for the idea that some of the impairments in social cognition seen in patients with autism may result from dysfunction of the amygdala.

The amygdala is involved in the normal facilitation of memory by emotion, but the separate contributions of the left and right amygdala to memory for verbal or nonverbal emotional material have not been investigated. Fourteen patients with damage to the medial temporal lobe including the amygdala (seven left, seven right), 18 brain-damaged, and 36 normal controls were exposed to emotional and neutral pictures accompanied by verbal narratives. Memory for both narratives and pictures was assessed with a free recall test 24 h later. Subjects with left amygdala damage failed to show the normally robust enhancement of memory for verbal and nonverbal emotional stimuli. The group with right amygdala damage showed the normal pattern of facilitation of memory by emotion for both verbal and nonverbal stimuli despite an overall reduction in memory performance. Furthermore, subjects with left amygdala damage were disproportionately impaired on memory for emotional narratives as compared with memory for emotional pictures. The latter finding offers partial support for a lateralized and material-specific pattern of the amygdala's contribution to emotional memory.

In humans, the emotional nature of stimuli appears to have a complex influence on long-term declarative memory for those stimuli: Whereas emotion enhances memory for gist, it may suppress memory for detail. On the basis of prior studies, the authors hypothesized that the amygdala helps mediate the above 2 effects. Long-term memory for gist and for visual detail of aversive and neutral scenes was assessed in 20 subjects with unilateral amygdala damage and 1 rare subject with bilateral amygdala damage. Comparisons with 2 control groups (15 brain-damaged and 47 healthy) provided evidence that bilateral, but not unilateral, damage to the amygdala results in poorer memory for gist but superior memory for visual details. The pattern of findings provides preliminary support for the idea that the amygdala may help filter the encoding of relevant information from stimuli that signal threat or danger.

Case studies of patients with bilateral amygdala damage and functional imaging studies of normal individuals have demonstrated that the amygdala plays a critical role in encoding emotionally arousing stimuli into long-term declarative memory. However, several issues remain poorly understood: the separate roles of left and right amygdala, the time course over which the amygdala participates in memory consolidation, and the type of knowledge structures it helps consolidate. We investigated these questions in eight subjects with unilateral amygdala damage, using several different measures. For comparison, our main task used stimuli identical to those used previously to investigate emotional declarative memory in patients with bilateral amygdala damage. Contrasts with both brain-damaged and normal control groups showed that subjects with left amygdala damage were impaired in their memory for emotional stimuli, despite entirely normal memory for neutral stimuli (because of a number of caveats, the findings from subjects with right amygdala damage were less clear). Follow-up experiments suggested that the normal facilitation of memory for emotional stimuli may develop over an extended time course (>30 min), consistent with prior findings, and that the specific impairment we report may depend in part on the lexical nature of the task used (written questionnaire). We stress the complex and temporally extended nature of memory consolidation and suggest that the amygdala may influence specific components of this process.

Bilateral damage to the human amygdala impairs retrieval of emotional and social information from faces. An important unanswered question concerns the specificity of the impairment for faces. To address this question, we examined preferences for a broad class of visual stimuli in two subjects with complete bilateral amygdala damage, both of whom were impaired in judgments of faces. Relative to controls, the subjects showed a positive bias for simple nonsense figures, color patterns, three-dimensional-looking objects and landscapes. The impairment was most pronounced in regard to those stimuli that are normally liked the least. The human amygdala thus appears to play a general role in guiding preferences for visual stimuli that are normally judged to be aversive.

Bilateral damage to the amygdala in a variety of animal species can impair emotional reactions to stimuli in several sensory modalities. Such damage in humans impairs visual recognition of emotion in facial expressions, but possible impairments in modalities other than vision have not been sufficiently explored. We examined two subjects with complete bilateral amygdala damage, and seven with unilateral amygdala damage, on a standardized task of emotional prosody recognition. The data were compared to those from 15 brain-damaged and from 14 normal control subjects. One of the bilateral amygdala subjects, whose lesions were restricted to the amygdala, was entirely normal in recognizing emotion in prosody on all tasks, the other, whose damage included substantial lesions also in extra-amygdalar structures, especially in right hemisphere, was normal on most, albeit not all, measures of emotional prosody recognition. We suggest that the human amygdala's role in recognizing emotion in prosody may not be as critical as it is for facial expressions, and that extra-amygdalar structures in right hemisphere may be more important for recognizing emotional prosody. It remains possible that recognition of emotion in classes of auditory stimuli other than prosody will require the amygdala.

Findings from several case studies have shown that bilateral amygdala damage impairs recognition of emotions in facial expressions, especially fear. However, one study did not find such an impairment, and, in general, comparison across studies has been made difficult because of the different stimuli and tasks employed. In a collaborative study to facilitate such comparisons, we report here the recognition of emotional facial expressions in nine subjects with bilateral amygdala damage, using a sensitive and quantitative assessment. Compared to controls, the subjects as a group were significantly impaired in recognizing fear, although individual performances ranged from severely impaired to essentially normal. Most subjects were impaired on several negative emotions in addition to fear, but no subject was impaired in recognizing happy expressions. An analysis of response consistency showed that impaired recognition of fear could not be attributed simply to mistaking fear for another emotion. While it remains unclear why some subjects with amygdala damage included here are not impaired on our task, the results overall are consistent with the idea that the amygdala plays an important role in triggering knowledge related to threat and danger signaled by facial expressions.

Studies in animals have implicated the amygdala in emotional and social behaviours, especially those related to fear and aggression. Although lesion and functional imaging studies in humans have demonstrated the amygdala's participation in recognizing emotional facial expressions, its role in human social behaviour has remained unclear. We report here our investigation into the hypothesis that the human amygdala is required for accurate social judgments of other individuals on the basis of their facial appearance. We asked three subjects with complete bilateral amygdala damage to judge faces of unfamiliar people with respect to two attributes important in real-life social encounters: approachability and trustworthiness. All three subjects judged unfamiliar individuals to be more approachable and more trustworthy than did control subjects. The impairment was most striking for faces to which normal subjects assign the most negative ratings: unapproachable and untrustworthy looking individuals. Additional investigations revealed that the impairment does not extend to judging verbal descriptions of people. The amygdala appears to be an important component of the neural systems that help retrieve socially relevant knowledge on the basis of facial appearance.

We have previously reported that bilateral amygdala damage in humans compromises the recognition of fear in facial expressions while leaving intact recognition of face identity (Adolphs et al., 1994). The present study aims at examining questions motivated by this finding. We addressed the possibility that unilateral amygdala damage might be sufficient to impair recognition of emotional expressions. We also obtained further data on our subject with bilateral amygdala damage, in order to elucidate possible mechanisms that could account for the impaired recognition of expressions of fear. The results show that bilateral, but not unilateral, damage to the human amygdala impairs the processing of fearful facial expressions. This impairment appears to result from an insensitivity to the intensity of fear expressed by faces. We also confirmed a double dissociation between the recognition of facial expressions of fear, and the recognition of identity of a face: these two processes can be impaired independently, lending support to the idea that they are subserved in part by anatomically separate neural systems. Based on our data, and on what is known about the amygdala's connectivity, we propose that the amygdala is required to link visual representations of facial expressions, on the one hand, with representations that constitute the concept of fear, on the other. Preliminary data suggest the amygdala's role extends to both recognition and recall of fearful facial expressions.

A patient with selective bilateral damage to the amygdala did not acquire conditioned autonomic responses to visual or auditory stimuli but did acquire the declarative facts about which visual or auditory stimuli were paired with the unconditioned stimulus. By contrast, a patient with selective bilateral damage to the hippocampus failed to acquire the facts but did acquire the conditioning. Finally, a patient with bilateral damage to both amygdala and hippocampal formation acquired neither the conditioning nor the facts. These findings demonstrate a double dissociation of conditioning and declarative knowledge relative to the human amygdala and hippocampus.

Studies in animals have shown that the amygdala receives highly processed visual input, contains neurons that respond selectively to faces, and that it participates in emotion and social behaviour. Although studies in epileptic patients support its role in emotion, determination of the amygdala's function in humans has been hampered by the rarity of patients with selective amygdala lesions. Here, with the help of one such rare patient, we report findings that suggest the human amygdala may be indispensable to: (1) recognize fear in facial expressions; (2) recognize multiple emotions in a single facial expression; but (3) is not required to recognize personal identity from faces. These results suggest that damage restricted to the amygdala causes very specific recognition impairments, and thus constrains the broad notion that the amygdala is involved in emotion.

The role of the human amygdala in cross-modal associations was investigated in two subjects: SM-046, who had bilateral damage circumscribed to the amygdala; and the patient known as Boswell, whose damage in both temporal lobes includes the amygdala and surrounding cortices. Neither subject was impaired on Tactile-Visual or Visual-Tactile cross-modal tasks using the Arc-Circle test, suggesting that the amygdala is not involved in cross-modal associations involving perceptually "equivalent" basic stimulus properties. On the other hand, the results are compatible with the amygdala's involvement in higher-order associations between exteroceptive sensory data and interoceptive data concerned with correlated somatic states.

We conducted an extensive neuropsychological investigation in a patient with bilateral amygdala damage due to Urbach-Wiethe disease. The patient had significant defects in nonverbal visual memory, in social behavior, and in "executive control" functions, findings consistent with the proposal, based on experimental animal work, that the amygdala plays important roles in memory and in the modulation of social and emotional behavior. General intellect and language were normal. A psychophysiological study showed that she had normal electrodermal activity (skin conductance responses), an important finding in view of the role that has been attributed to the amygdala in the central control of autonomic responses.

Several lines of evidence have suggested that the amygdala is a crucial component of the anatomical network that mediates the skin conductance orienting response (SCOR). In this study, the electrodermal activity of a patient whose entire amygdaloid complex had been destroyed bilaterally, and of 7 age- and gender-matched controls, was recorded under the same experimental conditions. The results indicate unequivocally that the subject could generate normal skin conductance and SCORs, in response to stimuli of different sensory modalities and configurations. This suggests that the amygdala is not a necessary component of the neural network underlying SCORs and that there are alternate neural units and pathways that link sensory cortices to autonomic effectors.