Neuron
Volume 109, Issue 11, 2 June 2021, Pages 1848-1860.e8
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Article
Coordination of escape and spatial navigation circuits orchestrates versatile flight from threats

https://doi.org/10.1016/j.neuron.2021.03.033Get rights and content
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Highlights

  • The dorsal premammillary nucleus (PMd) controls versatile and panic-related flight

  • The hypothalamic PMd nucleus recruits thalamic targets for escapes requiring navigation

  • The PMd engages brain stem targets for context-specific and panic-related escapes

  • Other defense-related hypothalamic nuclei only control simple flight actions in mice

Summary

Naturalistic escape requires versatile context-specific flight with rapid evaluation of local geometry to identify and use efficient escape routes. It is unknown how spatial navigation and escape circuits are recruited to produce context-specific flight. Using mice, we show that activity in cholecystokinin-expressing hypothalamic dorsal premammillary nucleus (PMd-cck) cells is sufficient and necessary for context-specific escape that adapts to each environment’s layout. In contrast, numerous other nuclei implicated in flight only induced stereotyped panic-related escape. We reasoned the dorsal premammillary nucleus (PMd) can induce context-specific escape because it projects to escape and spatial navigation nuclei. Indeed, activity in PMd-cck projections to thalamic spatial navigation circuits is necessary for context-specific escape induced by moderate threats but not panic-related stereotyped escape caused by perceived asphyxiation. Conversely, the PMd projection to the escape-inducing dorsal periaqueductal gray projection is necessary for all tested escapes. Thus, PMd-cck cells control versatile flight, engaging spatial navigation and escape circuits.

Keywords

Predator
Escape
Panic
Fear
Dorsolateral periaqueductal gray
Dorsal premammillary nucleus
anterior medial ventral thalamus
hypercapnia
calcium imaging
optogenetics

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These authors contributed equally

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