Periaqueductal Gray Neuronal Activities Underlie Different Aspects of Defensive Behaviors

Abstract

Defense is a basic survival mechanism when animals face danger. Previous studies have suggested that the midbrain periaqueductal gray (PAG) is essential for the generation of defensive reactions. Here we showed that optogenetic activation of neurons in the PAG in mice was sufficient to induce a series of defensive responses (including running, freezing, and avoidance). However, the endogenous neural dynamics of the PAG underlying defensive behaviors still remain elusive. Using chronic extracellular recording, we recorded the spiking activities of PAG neurons in freely behaving mice exposed to natural threats (rats). We observed that there exist distinct neuronal subsets within the PAG participating in respective detection (risk assessment) and response (flight) aspects of defensive behaviors. Our results demonstrate the important role of PAG neuronal activities in the control of different aspects of defensive behaviors, and provide novel insights for investigating defense from an electrophysiological perspective.

Significance statement: Defense is crucial for animals' survival in nature. Here, using optogenetic stimulation and in vivo recording in behaving mice reacting to threats, we explored the role of the midbrain periaqueductal gray (PAG) in defense. We show that optogenetic activation of PAG neurons is sufficient to elicit different aspects of defensive responses. Consistently, the present study provides in vivo evidence demonstrating that activity of the population of dorsal PAG neurons is activated during defense. Also, different subpopulations of units recorded in the dorsal PAG participate in distinct aspects of defensive behaviors. These findings help us understand the role of the PAG in animal behavior at the single neuron level.

Keywords: defensive behavior; electrophysiology; innate behavior; optogenetics; periaqueductal gray.