The human amygdala and the emotional evaluation of sensory stimuli

Abstract

A wealth of animal data implicates the amygdala in aspects of emotional processing. In recent years, functional neuroimaging and neuropsychological studies have begun to refine our understanding of the functions of the amygdala in humans. This literature offers insights into the types of stimuli that engage the amygdala and the functional consequences that result from this engagement. Specific conclusions and hypotheses include: (1) the amygdala activates during exposure to aversive stimuli from multiple sensory modalities; (2) the amygdala responds to positively valenced stimuli, but these responses are less consistent than those induced by aversive stimuli; (3) amygdala responses are modulated by the arousal level, hedonic strength or current motivational value of stimuli; (4) amygdala responses are subject to rapid habituation; (5) the temporal characteristics of amygdala responses vary across stimulus categories and subject populations; (6) emotionally valenced stimuli need not reach conscious awareness to engage amygdala processing; (7) conscious hedonic appraisals do not require amygdala activation; (8) activation of the amygdala is associated with modulation of motor readiness, autonomic functions, and cognitive processes including attention and memory; (9) amygdala activations do not conform to traditional models of the lateralization of emotion; and (10) the extent and laterality of amygdala activations are related to factors including psychiatric status, gender and personality. The strengths and weakness of these hypotheses and conclusions are discussed with reference to the animal literature.

Introduction

Neurobehavioral theorists have frequently argued that the amygdala plays a central role in the emotional processing of sensory stimuli. Electrophysiological, neuropharmacological, and lesion studies in animals, have all provided support for the involvement of the amygdala in both the evaluation and response to emotionally salient stimuli. However, there exists a strong need for human data. The relative distribution of sensory representations clearly differs across species. The primate amygdala receives a far greater input from cortical areas including auditory and visual sensory areas than is observed in other mammals such as rodents and cats [194]. These differences appear to have direct functional consequences for the sensory representations received or processed by the amygdala [121]. For instance, over a third of rodent amygdala cells respond to odorants [62], whereas only a very limited and nuclei-specific group of amygdala cells respond to odorants in humans [122]. Even among primate species, there exist differences in the sensory processing of the amygdala, with humans showing less frequent responses to simple auditory or visual stimuli than is seen in monkeys [212], [248], [303]. Additionally, some aspects of amygdala processing may be uniquely developed or expressed in humans, due to our well-developed use of language and other cognitive abilities. Finally, only human’s can directly report on their subjective reactions to stimuli.

With the advent of positron emission tomography (PET), and more recently functional magnetic resonance imaging (fMRI), an increasing body of literature addresses the role of the amygdala in the processing of emotionally salient stimuli in humans. Simultaneously, neurologists and neuropsychologists have begun to utilize sophisticated paradigms to delineate the specific aspects of emotional processing that are affected by amygdala lesions. Taken together, these two lines of inquiry lay the groundwork for refining our theories of amygdala functioning. This article provides an overview of this emerging literature and outlines several of the unique insights provided by this research.