Time-Resolved Fast Mammalian Behavior Reveals the Complexity of Protective Pain Responses

Publication date: 5 July 2017
Source:Cell Reports, Volume 20, Issue 1
Author(s): Liam E. Browne, Alban Latremoliere, Brendan P. Lehnert, Alyssa Grantham, Catherine Ward, Chloe Alexandre, Michael Costigan, Frédéric Michoud, David P. Roberson, David D. Ginty, Clifford J. Woolf
Potentially harmful stimuli are detected at the skin by nociceptor sensory neurons that drive rapid protective withdrawal reflexes and pain. We set out to define, at a millisecond timescale, the relationship between the activity of these sensory neurons and the resultant behavioral output. Brief optogenetic activation of cutaneous nociceptors was found to activate only a single action potential in each fiber. This minimal input was used to determine high-speed behavioral responses in freely behaving mice. The localized stimulus generated widespread dynamic repositioning and alerting sub-second behaviors whose nature and timing depended on the context of the animal and its position, activity, and alertness. Our findings show that the primary response to injurious stimuli is not limited, fixed, or localized, but is dynamic, and that it involves recruitment and gating of multiple circuits distributed throughout the central nervous system at a sub-second timescale to effectively both alert to the presence of danger and minimize risk of harm.

Graphical abstract

Teaser

Browne et al. find that the responses evoked by noxious stimuli, when examined at a millisecond resolution, are not fixed, localized, or limited to reflex withdrawal but are instead coordinated globally across the body in a sub-second time frame to alert the animal and limit potential harm.


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