A medullary centre for lapping in mice

Bowen Dempsey,Christo Goridis,Carmen Birchmeier,Evan R Harrell,Harry Carey,Séverine Diem,Simon Mcmullan,Selvee Sungeelee,Auguste Genovesio,Jean-François Brunet,Sandra Autran,James F A Poulet,Phillip Bokiniec,Zoubida Chettouh,Gilles Fortin

doi:10.1038/s41467-021-26275-y

Abstract

It has long been known that orofacial movements for feeding can be triggered, coordinated, and often rhythmically organized at the level of the brainstem, without input from higher centers. We uncover two nuclei that can organize the movements for ingesting fluids in mice. These neuronal groups, IRtPhox2b and Peri5Atoh1, are marked by expression of the pan-autonomic homeobox gene Phox2b and are located, respectively, in the intermediate reticular formation of the medulla and around the motor nucleus of the trigeminal nerve. They are premotor to all jaw-opening and tongue muscles. Stimulation of either, in awake animals, opens the jaw, while IRtPhox2b alone also protracts the tongue. Moreover, stationary stimulation of IRtPhox2b entrains a rhythmic alternation of tongue protraction and retraction, synchronized with jaw opening and closing, that mimics lapping. Finally, fiber photometric recordings show that IRtPhox2b is active during volitional lapping. Our study identifies one of the subcortical nuclei underpinning a stereotyped feeding behavior.

Highlights

It has long been known that orofacial movements for feeding can be triggered, coordinated, and often rhythmically organized at the level of the brainstem, without input from higher centers
The reticular formation has slowly emerged from “localizatory nihilism”[2], and regions defined by stereotaxy [e.g., ref. 3], or cell groups defined by their projections [e.g., ref. 4] have been implicated in a variety of roles: premotor neurons to orofacial or respiratory muscles[5, 6], and— underpinning the sophisticated residual behaviors observed in decerebrate animals7—rhythm and pattern generators for chewing, whisking, breathing, and sighing[3, 5, 8,9,10,11]
The expression landscape of Phox2b is strikingly unified by physiology: most Phox2b neurons studied to date, partake in the sensorimotor reflexes of the autonomic nervous system, that control bodily homeostasis[20]

Summary

Introduction

It has long been known that orofacial movements for feeding can be triggered, coordinated, and often rhythmically organized at the level of the brainstem, without input from higher centers. An apparent exception is branchial motor neurons, that motorize the face and neck[1, 21] but their kinship to visceral circuits, aptly highlighted by their alternative name of “special visceral”, is revealed by their exclusive ancestral functions in aquatic vertebrates, in feeding and breathing— visceral To this broadened picture of the visceral nervous system, in charge of vital functions and maintenance of the interior milieu, we add two groups of Phox2b interneurons, located in the reticular formation of the hindbrain, that are premotor to orofacial muscles and can command licking or lapping, a rhythmic feeding behavior essential for the intake of liquids in many terrestrial vertebrates

Methods

Results

Conclusion