Similar neural activity during fear and disgust in the rat basolateral amygdala.

Steven J Shabel,Victoria Powell,Will Schairer,Patricia H Janak,Rachel J Donahue,Hans P Op De Beeck

doi:10.1371/journal.pone.0027797

Abstract

Much research has focused on how the amygdala processes individual affects, yet little is known about how multiple types of positive and negative affects are encoded relative to one another at the single-cell level. In particular, it is unclear whether different negative affects, such as fear and disgust, are encoded more similarly than negative and positive affects, such as fear and pleasure. Here we test the hypothesis that the basolateral nucleus of the amygdala (BLA), a region known to be important for learned fear and other affects, encodes affective valence by comparing neuronal activity in the BLA during a conditioned fear stimulus (fear CS) with activity during intraoral delivery of an aversive fluid that induces a disgust response and a rewarding fluid that induces a hedonic response. Consistent with the hypothesis, neuronal activity during the fear CS and aversive fluid infusion, but not during the fear CS and rewarding fluid infusion, was more similar than expected by chance. We also found that the greater similarity in activity during the fear- and disgust-eliciting stimuli was specific to a subpopulation of cells and a limited window of time. Our results suggest that a subpopulation of BLA neurons encodes affective valence during learned fear, and furthermore, within this subpopulation, different negative affects are encoded more similarly than negative and positive affects in a time-specific manner.

Highlights

The basolateral nucleus of the amygdala (BLA) is important for affective processing [1,2,3,4,5] and has a well-established role in the acquisition and expression of Pavlovian fear memories [6]
Test sessions consisted of three parts – 20 fear conditioning trials, 20 rewarding fluid infusions, and 20 aversive fluid infusions (Fig. 1B and Fig. S1) – and were conducted while rats were water restricted
In this study we tested and confirmed a critical prediction of the hypothesis that the BLA encodes emotional valence: that neuronal activity during two different affects of the same valence - fear and disgust - is more similar than neuronal activity during two affects of different valence – fear and pleasure

Summary

Introduction

The basolateral nucleus of the amygdala (BLA) is important for affective processing [1,2,3,4,5] and has a well-established role in the acquisition and expression of Pavlovian fear memories [6]. Fear conditioning changes the responses of many neurons in the BLA to a conditioned fear stimulus (CS) [7], consistent with affective valence encoding [8,9,10], these neuronal responses could encode other attributes of the stimulus, including the sensory properties of the outcome it predicts [11,12], its arousing or activating properties [9,10,13,14,15], and/or the discrete affect induced by the stimulus (i.e., fear). If the BLA encodes affective valence during learned fear, neuronal activity during the fear CS should be more similar to neuronal activity during the aversive fluid infusion than the rewarding fluid infusion Note that because both the valencecongruent and valence-incongruent comparisons compare two different affects, any differences in the comparisons cannot be attributed to a simple change in affect

Methods

Results

Conclusion