Abstract

SummaryAnimals can choose to act upon, or to ignore, sensory stimuli, depending on circumstance and prior knowledge. This flexibility is thought to depend on neural inhibition, through suppression of inappropriate and disinhibition of appropriate actions. Here, we identified the ventral lateral geniculate nucleus (vLGN), an inhibitory prethalamic area, as a critical node for control of visually evoked defensive responses in mice. The activity of vLGN projections to the medial superior colliculus (mSC) is modulated by previous experience of threatening stimuli, tracks the perceived threat level in the environment, and is low prior to escape from a visual threat. Optogenetic stimulation of the vLGN abolishes escape responses, and suppressing its activity lowers the threshold for escape and increases risk-avoidance behavior. The vLGN most strongly affects visual threat responses, potentially via modality-specific inhibition of mSC circuits. Thus, inhibitory vLGN circuits control defensive behavior, depending on an animal’s prior experience and its anticipation of danger in the environment.

Highlights

  • Instinctive defensive behaviors are vital for survival because they enable fast reactions to environmental threats, such as escape from an approaching predator (Blanchard et al, 1990; Fotowat and Gabbiani, 2011; Yilmaz and Meister, 2013; Peek and Card, 2016; Branco and Redgrave, 2020)

  • Previous work has largely focused on inhibitory pathways in the basal ganglia (Mink, 1996; Nelson and Kreitzer, 2014), recent evidence suggests that inhibitory structures in the prethalamus, such as the zona incerta (ZI), could assert more direct control over responses to environmental stimuli (Chou et al, 2018; Zhao et al, 2019; Wang et al, 2019; Venkataraman et al, 2019; Hormigo et al, 2020; Ahmadlou et al, 2021)

  • The ventral lateral geniculate nucleus (vLGN) has a stronger effect on responses to visual, than to auditory, threats, and we find that this modality-specific effect on behavior is likely supported by a prominent, modality-specific influence of the vLGN on medial superior colliculus (SC) circuits

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Summary

Introduction

Instinctive defensive behaviors are vital for survival because they enable fast reactions to environmental threats, such as escape from an approaching predator (Blanchard et al, 1990; Fotowat and Gabbiani, 2011; Yilmaz and Meister, 2013; Peek and Card, 2016; Branco and Redgrave, 2020) These instinctive responses are surprisingly flexible and can be adapted or suppressed depending on environmental demands, the animal’s state, and prior knowledge (Evans et al, 2019). It is unclear how these circuits are regulated to enable flexible control of defensive behavior

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