Centralized gaze as an adaptive component of defensive states in humans

Abstract

Adequate defensive responding is crucial for mental health but scientifically not well understood. Specifically, it seems difficult to dissociate defense and approach states based on autonomic response patterns. We thus explored the robustness and threat-specificity of recently described oculomotor dynamics upon threat in anticipation of either threatening or rewarding stimuli in humans. While visually exploring naturalistic images, participants (50 per experiment) expected an inevitable, no, or avoidable shock (Experiment 1) or a guaranteed, no, or achievable reward (Experiment 2) that could be averted or gained by a quick behavioural response. We observed reduced heart rate (bradycardia), increased skin conductance, pupil dilation and globally centralized gaze when shocks were inevitable but, more pronouncedly, when they were avoidable. Reward trials were not associated with globally narrowed visual exploration, but autonomic responses resembled characteristics of the threat condition. While bradycardia and concomitant sympathetic activation reflect not only threat-related but also action-preparatory states independent of valence, global centralization of gaze seems a robust phenomenon during the anticipation of avoidable threat. Thus, instead of relying on single readouts, translational research in animals and humans should consider the multi-dimensionality of states in aversive and rewarding contexts, especially when investigating ambivalent, conflicting situations.