The neural basis of species-specific defensive behaviour in Peromyscus mice

Evading imminent predator threat is critical for survival. Effective
defensive strategies can vary, even between closely related species.
However, the neural basis of such species-specific behaviours is still
poorly understood. Here we find that two sister species of deer mice
(genus Peromyscus) show different responses to the same looming stimulus:
P. maniculatus, which occupies densely vegetated habitats, predominantly
escapes, while the open field specialist, P. polionotus, briefly freezes.
This difference arises from species-specific escape thresholds, is largely
context-independent, and can be triggered by both visual and auditory
threat stimuli. Using immunohistochemistry and electrophysiological
recordings, we find that although visual threat activates the superior
colliculus in both species, the role of the dorsal periaqueductal gray
(dPAG) in driving behaviour differs. While dPAG activity scales with
running speed in P. maniculatus, neural activity in the dPAG of P.
polionotus correlates poorly with movement, including during visually
triggered escape. Moreover, optogenetic activation of dPAG neurons elicits
acceleration in P. maniculatus but not P. polionotus, while their
chemogenetic inhibition during a looming stimulus delays escape onset in
P. maniculatus to match that of P. polionotus. Together, we trace
species-specific escape thresholds to a central circuit node, downstream
of peripheral sensory neurons, localizing an ecologically relevant
behavioural difference to a specific region of the mammalian brain.