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Ralph Adolphs

Publications and source records attributed to Ralph Adolphs.

At least 37 records · Page 2Linked to original sources

Analysis of single-unit responses to emotional scenes in human ventromedial prefrontal cortex.

Lesion and functional imaging studies in humans have shown that the ventral and medial prefrontal cortex is critically involved in the processing of emotional stimuli, but both of these methods have limited spatiotemporal resolution. Conversely, neurophysiological studies of emotion in nonhuman primates typically rely on stimuli that do not require elaborate cognitive processing. To begin bridging this gap, we recorded from a total of 267 neurons in the left and right orbital and anterior cingulate cortices of four patients who had chronically implanted depth electrodes for monitoring epilepsy. Peristimulus activity was recorded to standardized, complex visual scenes depicting neutral, pleasant, or aversive content. Recording locations were verified with postoperative magnetic resonance imaging. Using a conservative, multistep statistical evaluation, we found significant responses in 56 neurons; 16 of these were selective for only one emotion class, most often aversive. The findings suggest sparse and widely distributed processing of emotional value in the prefrontal cortex, with a predominance of responses to aversive stimuli.

Action Potentials↗

Impaired spontaneous anthropomorphizing despite intact perception and social knowledge.

Humans spontaneously imbue the world with social meaning: we see not only emotions and intentional behaviors in humans and other animals, but also anger in the movements of thunderstorms and willful sabotage in crashing computers. Converging evidence supports a role for the amygdala, a collection of nuclei in the temporal lobe, in processing emotionally and socially relevant information. Here, we report that a patient with bilateral amygdala damage described a film of animated shapes (normally seen as full of social content) in entirely asocial, geometric terms, despite otherwise normal visual perception. Control tasks showed that the impairment did not result from a global inability to describe social stimuli or a bias in language use, nor was a similar impairment observed in eight comparison subjects with damage to orbitofrontal cortex. This finding extends the role of the amygdala to the social attributions we make even to stimuli that are not explicitly social and, in so doing, suggests that the human capacity for anthropomorphizing draws on some of the same neural systems as do basic emotional responses.

Amygdala↗

Neuroanatomical substrates of social cognition dysfunction in autism.

In this review article, we summarize recent progress toward understanding the neural structures and circuitry underlying dysfunctional social cognition in autism. We review selected studies from the growing literature that has used the functional neuroimaging techniques of cognitive neuroscience to map out the neuroanatomical substrates of social cognition in autism. We also draw upon functional neuroimaging studies with neurologically normal individuals and individuals with brain lesions to highlight the insights these studies offer that may help elucidate the search for the neural basis of social cognition deficits in autism. We organize this review around key brain structures that have been implicated in the social cognition deficits in autism: (1) the amygdala, (2) the superior temporal sulcus region, and (3) the fusiform gyrus. We review some of what is known about the contribution of each structure to social cognition and then review autism studies that implicate that particular structure. We conclude with a discussion of several potential future directions in the cognitive neuroscience of social deficits in autism.

Amygdala↗

Anteromedial temporal lobe damage blocks startle modulation by fear and disgust.

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.

Acoustic Stimulation↗

Emotional vision.

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Amygdala↗

Cortical regions for judgments of emotions and personality traits from point-light walkers.

Humans are able to use nonverbal behavior to make fast, reliable judgments of both emotional states and personality traits. Whereas a sizeable body of research has identified neural structures critical for emotion recognition, the neural substrates of personality trait attribution have not been explored in detail. In the present study, we investigated the neural systems involved in emotion and personality trait judgments. We used a type of visual stimulus that is known to convey both emotion and personality information, namely, point-light walkers. We compared the emotion and personality trait judgments made by subjects with brain damage to those made by neurologically normal subjects and then conducted a lesion overlap analysis to identify neural regions critical for these two tasks. Impairments on the two tasks dissociated: Some subjects were impaired at emotion recognition, but judged personality normally; other subjects were impaired on the personality task, but normal at emotion recognition. Moreover, these dissociations in performance were associated with damage to specific neural regions: Right somatosensory cortices were a primary focus of lesion overlap in subjects impaired on the emotion task, whereas left frontal opercular cortices were a primary focus of lesion overlap in subjects impaired on the personality task. These findings suggest that attributions of emotional states and personality traits are accomplished by partially dissociable neural systems.

Adult↗

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.

Brain Damage, Chronic↗

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.

Amygdala↗

Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala.

The amygdala is known to play an important role in conscious and unconscious processing of emotional and highly arousing stimuli. Neuroanatomical evidence suggests that the amygdala participates in the control of autonomic responses, such as skin conductance responses (SCRs), elicited by emotionally salient stimuli, but little is known regarding its functional role in such control. We investigated this issue by showing emotional visual stimuli of varying arousal to patients with left (n = 12), right (n = 8), and bilateral (n = 3) amygdala damage and compared their results with those from 38 normal controls. Stimuli were presented both subliminally (using backward masking) and supraliminally under lateralized presentation to one visual hemifield. We collected SCRs as a physiological index of emotional responses. Subjects subsequently rated each stimulus on valence and arousal under free viewing conditions. There were two key findings: (1) impaired overall SCR after right amygdala damage; and (2) impaired correlation of SCR with the rated arousal of the stimuli after left amygdala damage. The second finding was strengthened further by finding a positive correlation between the evoked SCR magnitude and postsurgery amygdala volume, indicating impaired autonomic responses with larger tissue damage. Bilateral amygdala damage resulted in severe impairments on both of the above measures. Our results provide support for the hypothesis that the left and right amygdalae subserve different functions in emotion processing: the left may decode the arousal signaled by the specific stimulus, whereas the right may provide a global level of autonomic activation triggered automatically by any arousing stimulus.

Adult↗

Investigating the cognitive neuroscience of social behavior.

Social cognitive neuroscience is a fledgling discipline that has already accrued an impressive body of data, but important questions remain regarding the theoretical constructs and methodological approaches that it utilizes. An overview of the papers in this special issue points to several key issues facing the field. We need a theoretical vocabulary that bridges three domains: our intuitive "folk" conceptions of other people, the explanations offered by social psychology, and the explanations offered by cognitive neuroscience. And we need a method that can extract common patterns across multiple studies, to complement strict hypothesis testing of individual studies. These issues can be addressed, in part, by giving theory and experiment equal time, and by fostering an interdisciplinary approach that includes neuroscience, psychology, philosophy, anthropology and allied disciplines.

Animals↗

Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions.

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.

Adult↗

Dissociable neural systems for recognizing emotions.

This study tested the hypothesis that the recognition of emotions would draw upon anatomically separable brain regions, depending on whether the stimuli were static or explicitly conveyed information regarding actions. We investigated the hypothesis in a rare subject with extensive bilateral brain lesions, patient B., by administering tasks that assessed recognition and naming of emotions from visual and verbal stimuli, some of which depicted actions and some of which did not. B. could not recognize any primary emotion other than happiness, when emotions were shown as static images or given as single verbal labels. By contrast, with the notable exception of disgust, he correctly recognized primary emotions from dynamic displays of facial expressions as well as from stories that described actions. Our findings are consistent with the idea that information about actions is processed in occipitoparietal and dorsal frontal cortices, all of which are intact in B.'s brain. Such information subsequently would be linked to knowledge about emotions that depends on structures mapping somatic states, many of which are also intact in B.'s brain. However, one of these somatosensory structures, the insula, is bilaterally damaged, perhaps accounting for B.'s uniformly impaired recognition of disgust (from both static and action stimuli). Other structures that are damaged in B.'s brain, including bilateral inferior and anterior temporal lobe and medial frontal cortices, appear to be critical for linking perception of static stimuli to recognition of emotions. Thus the retrieval of knowledge regarding emotions draws upon widely distributed and partly distinct sets of neural structures, depending on the attributes of the stimulus.

Affect↗

Selective effects of triazolam on memory for emotional, relative to neutral, stimuli: differential effects on gist versus detail.

Benzodiazepines are known to reduce learning and memory performance, presumably through their facilitation of GABAergic neurotransmission, but the effects of these drugs specifically on memory for emotional material has not been addressed in humans. The effects of a benzodiazepine (triazolam, 0.25 mg) on nonincidental memory for emotional stimuli were assessed in 20 healthy volunteers (10 female). Triazolam reduced the normally facilitative effect of emotion on memory. The drug specifically affected memory for the gist of stimuli while leaving detail memory relatively unaffected. This pattern of performance is similar to that seen in patients with amygdala damage. Results suggest an effect of GABAergic neurotransmission at the level of the amygdala on memory modulation.

Adult↗

Evidence for preserved emotional memory in normal older persons.

Emotion has been shown to have a modulatory effect on declarative memory. Normal aging is associated with a decline in declarative memory, but whether aging might affect the influence of emotion on memory has not been established. To investigate this, we administered a task that provides a detailed assessment of emotional memory to 80 neurologically normal adults ranging in age from 35 to 85 years. Across ages, memory performance was found to be modulated by the emotional significance of stimuli in a comparable manner (improved memory for gist, compromised memory for visual detail), despite an overall decline in memory performance with increasing age. The results raise the interesting possibility that aging has a differential effect on hippocampal versus amygdala function.

Adult↗

Cognitive neuroscience of human social behaviour.

We are an intensely social species--it has been argued that our social nature defines what makes us human, what makes us conscious or what gave us our large brains. As a new field, the social brain sciences are probing the neural underpinnings of social behaviour and have produced a banquet of data that are both tantalizing and deeply puzzling. We are finding new links between emotion and reason, between action and perception, and between representations of other people and ourselves. No less important are the links that are also being established across disciplines to understand social behaviour, as neuroscientists, social psychologists, anthropologists, ethologists and philosophers forge new collaborations.

Cognition↗

Is the human amygdala specialized for processing social information?

A number of studies in humans and other animals has confirmed the amygdala's role in modulating cognition and behavior on the basis of a stimulus' motivational, emotional, and social attributes. This raises the question of how these attributes are related: is social information processing reducible to motivational processing? Some recent data suggest the possibility that the amygdala's primitive function may be motivational processing that is domain-general, but that its function in primates, and especially humans, may have evolved to process social information specifically. While the issue is unresolved, future experiments could provide additional support.

Amygdala↗

EMPATH: a neural network that categorizes facial expressions.

There are two competing theories of facial expression recognition. Some researchers have suggested that it is an example of "categorical perception." In this view, expression categories are considered to be discrete entities with sharp boundaries, and discrimination of nearby pairs of expressive faces is enhanced near those boundaries. Other researchers, however, suggest that facial expression perception is more graded and that facial expressions are best thought of as points in a continuous, low-dimensional space, where, for instance, "surprise" expressions lie between "happiness" and "fear" expressions due to their perceptual similarity. In this article, we show that a simple yet biologically plausible neural network model, trained to classify facial expressions into six basic emotions, predicts data used to support both of these theories. Without any parameter tuning, the model matches a variety of psychological data on categorization, similarity, reaction times, discrimination, and recognition difficulty, both qualitatively and quantitatively. We thus explain many of the seemingly complex psychological phenomena related to facial expression perception as natural consequences of the tasks' implementations in the brain.

Discrimination, Psychological↗

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.

Adult↗