A feedforward brainstem parasympathetic circuit recruits tongue blood flow during licking

Abstract

Blood perfusion is essential for muscle function. Licking, however, is a brief burst of behavior, and the reactive blood-flow systems that supply skeletal muscle — which respond to the metabolic byproducts of muscle activity — may be poorly suited to such fast, intermittent demands. Here we show that the tongue solves this problem with a dynamic feedforward parasympathetic circuit that recruits blood flow to support licking.

The tongue receives parasympathetic input from a VIP-positive subpopulation of the superior salivatory nucleus (SSN^VIP), a brainstem preganglionic parasympathetic nucleus that projects onto postganglionic parasympathetic neurons resident within the tongue (intralingual parasympathetic neurons, ILPNs). Chemogenetic activation of SSNVIP increased tongue blood flow in anesthetized mice, without inducing detectable saliva secretion. In behaving animals, chemogenetic activation increased licking amplitude and reduced its trial-to-trial variability, whereas silencing SSNVIP or ILPNVIP reduced licks per bout and tongue movement velocity. Fiber photometry showed that SSNVIP neurons increased their activity before the onset of tongue protrusion, regardless of spout contact or auditory cue, consistent with feedforward recruitment of the circuit.  

Together, these results reveal that licking is generated by the coordinated activity of two systems — a brainstem motor circuit that drives the movement and an autonomic circuit that directs blood flow to support it.