Elsevier

Biological Psychiatry

Volume 54, Issue 5, 1 September 2003, Pages 504-514
Biological Psychiatry

Review
Neurobiology of emotion perception I: the neural basis of normal emotion perception

https://doi.org/10.1016/S0006-3223(03)00168-9Get rights and content

Abstract

There is at present limited understanding of the neurobiological basis of the different processes underlying emotion perception. We have aimed to identify potential neural correlates of three processes suggested by appraisalist theories as important for emotion perception: 1) the identification of the emotional significance of a stimulus; 2) the production of an affective state in response to 1; and 3) the regulation of the affective state. In a critical review, we have examined findings from recent animal, human lesion, and functional neuroimaging studies. Findings from these studies indicate that these processes may be dependent upon the functioning of two neural systems: a ventral system, including the amygdala, insula, ventral striatum, and ventral regions of the anterior cingulate gyrus and prefrontal cortex, predominantly important for processes 1 and 2 and automatic regulation of emotional responses; and a dorsal system, including the hippocampus and dorsal regions of anterior cingulate gyrus and prefrontal cortex, predominantly important for process 3. We suggest that the extent to which a stimulus is identified as emotive and is associated with the production of an affective state may be dependent upon levels of activity within these two neural systems.

Introduction

Critical to survival is the ability to identify quickly in the environment emotionally salient information, including danger and reward, and to form rapid and appropriate behavioral responses (Darwin 1872/1965). Although it is clear that the presence of an emotion involves physiologic arousal, appraisal, subjective experience, expression, and goal-directed behavior (Plutchik 1984), there is at present no generally accepted theoretical framework for human emotion and limited understanding of the neurobiological basis of the different processes underlying emotion perception. In this critical review, by examining the findings from recent animal, human lesion, and functional neuroimaging studies, we have aimed to identify the neural basis of a series of different neuropsychological processes important to the understanding of normal human emotional behavior.

Section snippets

Neuropsychological processes underlying emotion perception

Early theories proposed to explain the neuropsychological basis of emotion perception Cannon 1929, James 1884 emphasized the importance of feedback from bodily responses to an emotionally salient stimulus in determining the nature and extent of emotional feeling, but they did not distinguish between the identification of the emotive stimulus and the affective state produced in response to this. Appraisalist theories of emotion Arnold 1960, Lazarus 1991, and current researchers (Clore and Ortony

Animal studies

Many of these studies have been helpful in determining neural regions associated with behavioral responses to emotive stimuli (i.e., the combination of processes 1 and 2), whereas other studies have attempted to examine regions associated predominantly with process 1. These have demonstrated the importance of the amygdala in the initial response to emotionally salient stimuli. Cells in the amygdala responding selectively to faces and eye gaze direction have been identified in studies of

Animal studies

The existence of brain regions specialized for reward processing was initially suggested by studies showing that rats responded operantly to stimulation of specific sites to the exclusion of other activities (Olds and Milner 1954). These included the midbrain dopaminergic projections from the ventral tegmental area into the nucleus accumbens shell region and the medial prefrontal cortex (Spanagel and Weiss 1999). In primates, regions important for reward processing have been identified as the

Animal studies

Studies have implicated the medial prefrontal cortex in the regulation of affective state and emotional behavior (Mega et al 1997). This region is strategically located between two broad trends or compartments in cortical evolution (Sanides 1970). The ventrolateral trend is reactive-based, operates by feedback, and is derived from archicortex (olfactory cortex). In addition to the response to emotional stimuli, ventral prefrontal regions appear to have a role in emotional behavioral regulation

Conclusions: neural systems for emotion perception

In this review, we have described findings from studies employing a variety of techniques and specific experimental paradigms, which have helped to increase understanding of the neural basis of neuropsychological processes important for emotion perception, namely: the identification of the emotional significance of an environmental stimulus; the production of an affective state and emotional behavior; and the regulation of the affective state and emotional behavior, allowing the generation of

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