Abstract

Animals respond to environmental threats, e.g. looming visual stimuli, with innate defensive behaviors such as escape and freezing. The key neural circuits that participate in the generation of such dimorphic defensive behaviors remain unclear. Here we show that the dimorphic behavioral patterns triggered by looming visual stimuli are mediated by parvalbumin-positive (PV+) projection neurons in mouse superior colliculus (SC). Two distinct groups of SC PV+ neurons form divergent pathways to transmit threat-relevant visual signals to neurons in the parabigeminal nucleus (PBGN) and lateral posterior thalamic nucleus (LPTN). Activations of PV+ SC-PBGN and SC-LPTN pathways mimic the dimorphic defensive behaviors. The PBGN and LPTN neurons are co-activated by looming visual stimuli. Bilateral inactivation of either nucleus results in the defensive behavior dominated by the other nucleus. Together, these data suggest that the SC orchestrates dimorphic defensive behaviors through two separate tectofugal pathways that may have interactions.

Highlights

  • Animals respond to environmental threats, e.g. looming visual stimuli, with innate defensive behaviors such as escape and freezing

  • Defensive behavior with a positive LSIduring stimuli value and negative LSIafter stimuli value was defined as an escape-freezing pattern (Type I), whereas that with negative values for both LSIduring stimuli and LSIafter stimuli was defined as a freezing-only pattern (Type II)

  • A small proportion of mice (14/58, ~24%) showed the Type II pattern. These data indicate that looming visual stimuli trigger stereotyped dimorphic defensive behavioral patterns in mice

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Summary

Introduction

Animals respond to environmental threats, e.g. looming visual stimuli, with innate defensive behaviors such as escape and freezing. Innate defensive behaviors triggered by environmental threats play a critical role in animal survival[1,2] Among these behaviors, fleeing and freezing are fundamental forms in natural and laboratory conditions[3,4]. Early seminal studies of the SC indicated that distinct defensive behavioral patterns can be triggered by stimulation at different sites in the SC27 These studies were followed by the identification of looming-sensitive cells in specific layers of the SC32. These behavioral and physiological data suggest that, among the intermingled diverse cell types in the SC21,33, a subset of neurons may detect looming visual stimuli and participate in the generation of dimorphic defensive behaviors. Our data indicate that the SC PV+ neurons orchestrate these dimorphic defensive behaviors with two divergent tectofugal visual pathways

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