The periaqueductal gray orchestrates sensory and motor circuits at multiple levels of the neuraxis

Stella Koutsikou, Thomas C. Watson, Jonathan J. Crook, J. Lianne Leith, Charlotte L. Lawrenson, Richard Apps*, Bridget M. Lumb

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

33 Citations (Scopus)
366 Downloads (Pure)

Abstract

The periaqueductal gray (PAG) coordinates behaviors essential to survival, including striking changes in movement and posture (e.g., escape behaviors in response to noxious stimuli vs freezing in response to fear-evoking stimuli). However, the neural circuits underlying the expression of these behaviors remain poorly understood. We demonstrate in vivo in rats that activation of the ventrolateral PAG (vlPAG) affects motor systems at multiple levels of the neuraxis through the following: (1) differential control of spinal neurons that forward sensory information to the cerebellum via spino-olivo-cerebellar pathways (nociceptive signals are reduced while proprioceptive signals are enhanced); (2) alterations in cerebellar nuclear output as revealed by changes in expression of Fos-like immunoreactivity; and (3) regulation of spinal reflex circuits, as shown by an increase in[1]-motoneuron excitability. The capacity to coordinate sensory and motor functions is demonstrated in awake, behaving rats, in which natural activation of the vlPAG in fear-conditioned animals reduced transmission in spino-olivo-cerebellar pathways during periods of freezing that were associated with increased muscle tone and thus motor outflow. The increase in spinal motor reflex excitability and reduction in transmission of ascending sensory signals via spinoolivo-cerebellar pathways occurred simultaneously.Wesuggest that the interactions revealed in the present study between the vlPAG and sensorimotor circuits could form the neural substrate for survival behaviors associated with vlPAG activation.

Original languageEnglish
Pages (from-to)14132-14147
Number of pages16
JournalJournal of Neuroscience
Volume35
Issue number42
DOIs
Publication statusPublished - 21 Oct 2015

Keywords

  • Cerebellum
  • Fear
  • Nociception
  • Periaqueductal grey
  • Proprioception
  • Spinal cord

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