Abstract

Animals can effortlessly adapt their behavior by generalizing from past aversive experiences, allowing to avoid harm in novel situations. We studied how visual information was sampled by eye-movements during this process called fear generalization, using faces organized along a circular two-dimensional perceptual continuum. During learning, one face was conditioned to predict a harmful event, whereas the most dissimilar face stayed neutral. This introduced an adversity gradient along one specific dimension, while the other, unspecific dimension was defined solely by perceptual similarity. Aversive learning changed scanning patterns selectively along the adversity-related dimension, but not the orthogonal dimension. This effect was mainly located within the eye region of faces. Our results provide evidence for adaptive changes in viewing strategies of faces following aversive learning. This is compatible with the view that these changes serve to sample information in a way that allows discriminating between safe and adverse for a better threat prediction.

Highlights

  • To avoid costly situations, animals must be able to rapidly predict future adversity based on previously learnt aversive associations [1], as well as actively sampled information from the environment

  • Eye movements can shed light on the global objectives of the nervous system, as they represent the final behavioral outcome of complex neuronal processes. They can provide important insights into systems level alterations induced by aversive learning, which is important to elucidate as many anxiety disorders are believed to result from an inability to form optimal aversive representations

  • Participants associated an aversive outcome with a given face positioned along a similarity continuum, thereby learning facial prototypes for adversity and safety

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Summary

Introduction

Animals must be able to rapidly predict future adversity based on previously learnt aversive associations [1], as well as actively sampled information from the environment. For aversive learning to be effective a careful balance between stimulus generalization and selectivity is needed [4,5] While generalization makes it possible to promptly deploy defensive behavior when similar situations are encountered anew [6,7,8], selectivity ensures that only truly aversive stimuli are recognized as aversive [9,10], avoiding costly false alarms. A central part of active exploration are eye-movements [12,13,14,15,16] which can rapidly determine what information is available in a scene for recognizing adversity [17] It is not known in how far representations of adversity interact with active exploration during viewing of complex visual information. We investigated this question by comparing exploration strategies during viewing of faces before and after aversive learning

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