Role of the amygdala in processing visual social stimuli

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Abstract

We review the evidence implicating the amygdala as a critical component of a neural network of social cognition, drawing especially on research involving the processing of faces and other visual social stimuli. We argue that, although it is clear that social behavioral representations are not stored in the amygdala, the most parsimonious interpretation of the data is that the amygdala plays a role in guiding social behaviors on the basis of socioenvironmental context. Thus, it appears to be required for normal social cognition. We propose that the amygdala plays this role by attentionally modulating several areas of visual and somatosensory cortex that have been implicated in social cognition, and in helping to direct overt visuospatial attention in face gaze. We also hypothesize that the amygdala exerts attentional modulation of simulation in somatosensory cortices such as supramarginal gyrus and insula. Finally, we argue that the term emotion be broadened to include increased attention to bodily responses and their representation in cortex.

Introduction

The amygdala has long been implicated in primate social cognition and behavior, due primarily to the well-known work by Kluver and Bucy (1939) and the studies by Kling and colleagues (Dicks et al., 1968; Kling, 1968, Kling, 1974; Kling et al., 1970, Kling et al., 1979; Brothers et al., 1990). An influential view of the amygdala emerging from early studies of its function was that it acts as a generative locus of social cognition and behavior, required to link the perception of any stimuli to information about their value to an organism (Weiskrantz, 1956). One interpretation of this view is that the amygdala is a primary source of social behavior, and the lack of a functioning amygdala would be expected to severely limit a primate's range of social responses, perhaps going so far as to eliminate some part or all of the social repertoire altogether. More recent findings challenge the view that the amygdala is required for basic social behaviors. Yet the question remains open whether the amygdala is a required component for normal social cognition. For example, is the amygdala necessary for the normal information processing associated with an organism's evaluation of a visual social stimulus, such as a facial expression (on which subsequent behaviors could then be based)? We will see that an answer to this question depends on a new consideration of evidence for the amygdala's role. The view we will present takes into consideration evidence regarding the amygdala's role in modulating autonomic arousal, new evidence regarding the amygdala's potential to affect visuospatial and visual object-based attention, and recent accounts that explain social cognition in terms of simulation theory. These newer developments have posed something of a puzzle for older theories of the amygdala. We will review some older findings first, and the framework that was based on them. Then we will introduce the new findings and framework, and end by proposing a framework describing the amygdala's function in recognizing the social value of stimuli.

Section snippets

Shifting views of the amygdala in social cognition

Studies of the primate amygdala began in the 1930s with Kluver and Bucy's well-known experiments in monkeys (Kluver and Bucy, 1937, Kluver and Bucy, 1997). Following large bitemporal lesions that encompassed the amygdala, the animals came to exhibit a constellation of impairments in recognizing the emotional and social meaning of stimuli—the so-called “psychic blindness” of Kluver–Bucy syndrome. Notably, the monkeys became exceptionally tame and placid, a behavioral abnormality that has been

Impaired social cognition in humans following amygdala damage

While the amygdala has been implicated in monkey social behavior for some time, it is only very recently that such a role has been established in humans, and that detailed hypotheses have been investigated regarding the underlying mechanisms. Here, we review evidence that the amygdala has a role in the recognition of emotion from faces, in interpreting eye gaze, and in more complex social judgments in humans. Two early studies showed that bilateral damage confined mainly to the amygdala

The amygdala influences early visual processing of faces and affective stimuli

There is abundant data regarding the cortical processing of faces, and such cortical processing presumably can serve to provide highly processed input to the amygdala. To briefly review this, functional magnetic resonance imaging (fMRI) studies have revealed an array of higher order visual cortical regions that are engaged in face processing, including the fusiform face area (FFA) in the fusiform gyrus, the face-sensitive area in the superior temporal sulcus (STS), and superior and middle

The amygdala influences face gaze

In addition to influencing visual processing even at very early stages, recent evidence suggests that the amygdala affects face gaze in a surprisingly direct manner (Adolphs et al., 2005). This is consistent with the amygdala's influence on visual processing and with previous work showing that the amygdala affects visual and visuospatial attention. Lesions of the amygdala, particularly of the left amygdala, seriously impair the attentional benefit in the perception of aversive words during an

The amygdala mediates autonomic arousal elicited by faces

The human amygdala was originally thought to have a key role in the generation of normal autonomic responses associated with orienting and arousal due to studies of amygdalectomized monkeys (Bagshaw and Benzies, 1968; Bagshaw and Coppock, 1968; Pribram et al., 1979). Monkeys with bilateral amygdalectomies fail to produce the expected changes in skin conductance response (SCR), heart rate, and respiratory rate in response to irregularly repeated sounds, while ear movements to the sounds are

The amygdala and simulation: somatosensory attention as a component of emotional response to faces in social judgment

So far, we have seen that the amygdala acts to influence key components of object-based visual processing, visuospatial attention, and autonomic responses during the processing of facial expressions in social judgment. One important component of emotion judgment not yet addressed in this scheme is systems that have been implicated by simulation theoretic approaches to social cognition (Gallese et al., 2004; Rizzolatti and Craighero, 2004, see also Keysers and Gazzola, this volume). We will

The new model for how the amygdala contributes to the recognition of emotion from visual social stimuli

We are now able to articulate a coherent view of the amygdala's action in judging emotion from a face. The story proceeds like this (Fig. 3): visual input to the amygdala, which can occur very rapidly via the pulvinar, results in initial modulation of subsequent visual inputs from visual cortex. Attentional modulation of somatosensory (i.e., putative simulation) cortex occurs so as to increase sensitivity to and selectivity for bodily responses and encoded emotional associations. Modulation of

Acknowledgments

The authors thank Fred Gosselin and Dirk Neumann for helpful discussions. This work was supported by grants from the National Institute of Mental Health, the Cure Autism New Foundation, and the Pfeiffer Research Foundation.

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