Impaired judgments of sadness but not happiness following bilateral amygdala damage

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

Dominance attributions following damage to the ventromedial prefrontal cortex

Damage to the human ventromedial prefrontal cortex (VM) can result in dramatic and maladaptive changes in social behavior despite preservation of most other cognitive abilities. One important aspect of social cognition is the ability to detect social dominance, a process of attributing from particular social signals another person's relative standing in the social world. To test the role of the VM in making attributions of social dominance, we designed two experiments: one requiring dominance judgments from static pictures of faces, the second requiring dominance judgments from film clips. We tested three demographically matched groups of subjects: subjects with focal lesions in the VM (n=15), brain-damaged comparison subjects with lesions excluding the VM (n=11), and a reference group of normal individuals with no history of neurological disease (n=32). Contrary to our expectation, we found that subjects with VM lesions gave dominance judgments on both tasks that did not differ significantly from those given by the other groups. Despite their grossly normal performance, however, subjects with VM lesions showed more subtle impairments specifically when judging static faces: They were less discriminative in their dominance judgments, and did not appear to make normal use of gender and age of the faces in forming their judgments. The findings suggest that, in the laboratory tasks we used, damage to the VM does not necessarily impair judgments of social dominance, although it appears to result in alterations in strategy that might translate into behavioral impairments in real life

Impaired recognition of social emotions following amygdala damage

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

Fear and the human amygdala

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

Economic Games Quantify Diminished Sense of Guilt in Patients with Damage to the Prefrontal Cortex

Damage to the ventromedial prefrontal cortex (VMPFC) impairs concern for other people, as reflected in the dysfunctional real-life social behavior of patients with such damage, as well as their abnormal performances on tasks ranging from moral judgment to economic games. Despite these convergent data, we lack a formal model of how, and to what degree, VMPFC lesions affect an individual's social decision-making. Here we provide a quantification of these effects using a formal economic model of choice that incorporates terms for the disutility of unequal payoffs, with parameters that index behaviors normally evoked by guilt and envy. Six patients with focal VMPFC lesions participated in a battery of economic games that measured concern about payoffs to themselves and to others: dictator, ultimatum, and trust games. We analyzed each task individually, but also derived estimates of the guilt and envy parameters from aggregate behavior across all of the tasks. Compared with control subjects, the patients donated significantly less and were less trustworthy, and overall our model found a significant insensitivity to guilt. Despite these abnormalities, the patients had normal expectations about what other people would do, and they also did not simply generate behavior that was more noisy. Instead, the findings argue for a specific insensitivity to guilt, an abnormality that we suggest characterizes a key contribution made by the VMPFC to social behavior

Searching for the neural causes of criminal behavior

All behavior is proximally caused by the brain, but the neural causes of most complex behaviors are still not understood. Much of our ignorance stems from the fact that complex behavior depends on distributed neural control. Unlike a reflex, where the arc from sensation to action can be traced through a few synapses, most volitional behavior involves a dense causal web through which stimuli, memories, beliefs, and other factors exert their effects. Disruption anywhere in this causal web can produce effects that are difficult to trace back to their origin. Against this background, the finding that focal lesions of the ventromedial prefrontal cortex could lead to immoral and even criminal behavior generated considerable surprise and interest (1, 2). While a number of rare cases have now been described in whom a focal lesion caused criminality, these are neither very consistent (the lesions occur in several different anatomical locations) nor at all reliable (only a small fraction of patients, for any lesion location, show criminal behavior). To explain the effects of a lesion on criminal behavior, we need to understand what it is that the lesion does to the rest of the brain, a network-level understanding of lesion effects now provided by the new study of Darby et al. in PNAS (3)

Model-based lesion mapping of cognitive control using the Wisconsin Card Sorting Test

The role of the frontal lobes in cognition and behavior has long been enigmatic. Over the past decade, computational models have provided a powerful approach to understanding cognition and decision-making. Here, we used a model-based approach to analyze data from a classical task used to assess frontal lobe function, the Wisconsin Card Sorting Test. We applied computational modeling and voxel-based lesion-symptom mapping in 328 patients with focal lesions, to uncover cognitive processes and neural correlates of test scores. Our results reveal that lesions in the right prefrontal cortex are associated with elevated perseverative errors and reductions in the model parameter of sensitivity to punishment. These findings indicate that the capacity to flexibly switch between task sets requires the detection of contingency changes, which are enabled by a sensitivity to punishment that reduces perseverative errors. We demonstrate the power of model-based approaches in understanding patterns of deficits on classical neuropsychological tasks

Impaired Emotional Declarative Memory Following Unilateral Amygdala Damage

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

Focal ventromedial prefrontal cortex damage impairs convergence in discourse

Conversational partners tend to converge (become more similar) on various speech and discourse characteristics, enhancing social affiliation. We examined convergence in the discourse of eight participants with bilateral ventromedial prefrontal cortex (VMPC) damage and eight healthy comparison participants (NC) each interacting with a clinician. Changes in total words, words/turn, and backchannels were assessed across the interaction by comparing the first ¼ and last ¼ of the session. Preliminary results suggest that convergence was displayed in NC interactions as conversational partners become more similar to one another across variables. In striking contrast, VMPC interactions did not display convergence across any variables