Temporal dynamics of amygdala response to emotion- and action-relevance

Raphael Guex,Patrik Vuilleumier,Bryan A Strange,Ryan J Murray,David Sander,Judith Domínguez-Borràs,Stephan Moratti,Laurent Spinelli,Margitta Seeck,Constantino Méndez-Bértolo

doi:10.1038/s41598-020-67862-1

Abstract

It has been proposed that the human amygdala may not only encode the emotional value of sensory events, but more generally mediate the appraisal of their relevance for the individual’s goals, including relevance for action or task-based needs. However, emotional and non-emotional/action-relevance might drive amygdala activity through distinct neural signals, and the relative timing of both kinds of responses remains undetermined. Here, we recorded intracranial event-related potentials from nine amygdalae of patients undergoing epilepsy surgery, while they performed variants of a Go/NoGo task with faces and abstract shapes, where emotion- and action-relevance were orthogonally manipulated. Our results revealed early amygdala responses to emotion facial expressions starting ~ 130 ms after stimulus-onset. Importantly, the amygdala responded to action-relevance not only with face stimuli but also with abstract shapes (squares), and these relevance effects consistently occurred in later time-windows (starting ~ 220 ms) for both faces and squares. A similar dissociation was observed in gamma activity. Furthermore, whereas emotional responses habituated over time, the action-relevance effect increased during the course of the experiment, suggesting progressive learning based on the task needs. Our results support the hypothesis that the human amygdala mediates a broader relevance appraisal function, with the processing of emotion-relevance preceding temporally that of action-relevance.

Highlights

The amygdala is a crucial component of brain circuits allowing swift reaction to threatening stimuli, an ability critical for adaptive behavior and survival[1,2]
Other views suggest that emotional signals are intimately related to the encoding of behavioral goal v alues[17]. This may occur both in the long-term perspective of biological needs, or in a more short-term perspective, conceptualized as information relevant to adjust behavior in order to perform a current t ask[9,10]. Indirect support to such relevance hypothesis has come from several functional magnetic resonance imaging studies using emotional stimuli, as well as non-emotional stimuli
This would accord with the relevance hypothesis postulating that a primary role of the amygdala is to compute the personal significance of an event, in relation to current goals and needs, so as to motivate adaptive actions and behaviors[4]

Summary

Introduction

The amygdala is a crucial component of brain circuits allowing swift reaction to threatening stimuli, an ability critical for adaptive behavior and survival[1,2]. Other views suggest that emotional signals (and associated stimulus processing in amygdala and connected regions) are intimately related to the encoding of behavioral goal v alues[17] This may occur both in the long-term perspective of biological needs, or in a more short-term perspective, conceptualized as information relevant to adjust behavior in order to perform a current t ask[9,10]. Several studies using non-emotional stimuli, such as letters or numbers previously associated with a particular taskdependent value, showed robust activation within the amygdala unrelated to any affective v alue[26,27] This would accord with the relevance hypothesis postulating that a primary role of the amygdala is to compute the personal significance of an event, in relation to current goals and needs, so as to motivate adaptive actions and behaviors[4]. Previous fMRI studies cannot shed light on this question since BOLD activity lacks the temporal resolution necessary to determine the exact dynamics underlying these processes

Methods

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Discussion

Conclusion