Dorsal premammillary projection to periaqueductal gray controls escape vigor from innate and conditioned threats

Elife. 2021 Sep 1:10:e69178. doi: 10.7554/eLife.69178.

Abstract

Escape from threats has paramount importance for survival. However, it is unknown if a single circuit controls escape vigor from innate and conditioned threats. Cholecystokinin (cck)-expressing cells in the hypothalamic dorsal premammillary nucleus (PMd) are necessary for initiating escape from innate threats via a projection to the dorsolateral periaqueductal gray (dlPAG). We now show that in mice PMd-cck cells are activated during escape, but not other defensive behaviors. PMd-cck ensemble activity can also predict future escape. Furthermore, PMd inhibition decreases escape speed from both innate and conditioned threats. Inhibition of the PMd-cck projection to the dlPAG also decreased escape speed. Intriguingly, PMd-cck and dlPAG activity in mice showed higher mutual information during exposure to innate and conditioned threats. In parallel, human functional magnetic resonance imaging data show that a posterior hypothalamic-to-dlPAG pathway increased activity during exposure to aversive images, indicating that a similar pathway may possibly have a related role in humans. Our data identify the PMd-dlPAG circuit as a central node, controlling escape vigor elicited by both innate and conditioned threats.

Keywords: dorsal premammillary nucleus; escape; fear; mouse; neuroscience; panic; periaqueductal gray; predator.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Animals
  • Behavior, Animal*
  • Brain Mapping
  • Cholecystokinin / genetics
  • Cholecystokinin / metabolism
  • Conditioning, Psychological*
  • Escape Reaction*
  • Fear*
  • Female
  • Humans
  • Hypothalamus, Posterior / diagnostic imaging
  • Hypothalamus, Posterior / metabolism
  • Hypothalamus, Posterior / physiology*
  • Magnetic Resonance Imaging
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neural Pathways / physiology
  • Optogenetics
  • Periaqueductal Gray / diagnostic imaging
  • Periaqueductal Gray / metabolism
  • Periaqueductal Gray / physiology*
  • Photic Stimulation
  • Rats
  • Rats, Long-Evans
  • Time Factors
  • Video Recording
  • Visual Perception
  • Young Adult

Substances

  • Cholecystokinin

Associated data

  • Dryad/10.5061/dryad.D19H5X