Ralph Adolphs

Abstract: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 atttributes. 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.

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.

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.

Recognizing emotion from facial expressions draws on diverse psychological processes implemented in a large array of neural structures. Studies using evoked potentials, lesions, and functional imaging have begun to elucidate some of the mechanisms. Early perceptual processing of faces draws on cortices in occipital and temporal lobes that construct detailed representations from the configuration of facial features. Subsequent recognition requires a set of structures, including amygdala and orbitofrontal cortex, that links perceptual representations of the face to the generation of knowledge about the emotion signaled, a complex set of mechanisms using multiple strategies. Although recent studies have provided a wealth of detail regarding these mechanisms in the adult human brain, investigations are also being extended to nonhuman primates, to infants, and to patients with psychiatric disorders.

Which brain regions are associated with recognition of emotional prosody? Are these distinct from those for recognition of facial expression? These issues were investigated by mapping the overlaps of co-registered lesions from 66 brain-damaged participants as a function of their performance in rating basic emotions. It was found that recognizing emotions from prosody draws on the right frontoparietal operculum, the bilateral frontal pole, and the left frontal operculum. Recognizing emotions from prosody and facial expressions draws on the right frontoparietal cortex, which may be important in reconstructing aspects of the emotion signaled by the stimulus. Furthermore, there were regions in the left and right temporal lobes that contributed disproportionately to recognition of emotion from faces or prosody, respectively.

The authors previously reported that normal subjects are better at discriminating happy from neutral faces when the happy face is located to the viewer's right of the neutral face; conversely, discrimination of sad from neutral faces is better when the sad face is shown to the left, supporting a role for the left hemisphere in processing positive valence and for the right hemisphere in processing negative valence. Here, the authors extend this same task to subjects with unilateral cerebral damage (31 right, 28 left). Subjects with right damage performed worse when discriminating sad faces shown on the left, consistent with the prior findings. However, subjects with either left or right damage actually performed superior to normal controls when discriminating happy faces shown on the left. The authors suggest that perception of negative valence relies preferentially on the right hemisphere, whereas perception of positive valence relies on both left and right hemispheres.