Mechanoreceptor synapses in the brainstem shape the central representation of touch

Brendan P Lehnert,Celine Santiago,Erica L Huey,Alan J Emanuel,Sophia Renauld,Nusrat Africawala,Ilayda Alkislar,Yang Zheng,Ling Bai,Charalampia Koutsioumpa,Jennifer T Hong,Alexandra R Magee,Christopher D Harvey,David D Ginty

doi:10.1016/j.cell.2021.09.023

Brendan P Lehnert, Celine Santiago + Show 12 more

Open Access

https://doi.org/10.1016/j.cell.2021.09.023

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Journal: Cell	Publication Date: Oct 1, 2021
Citations: 32	License type: cc-by

Affiliation: Howard Hughes Medical Institute, Harvard University

Abstract

Mammals use glabrous (hairless) skin of their hands and feet to navigate and manipulate their environment. Cortical maps of the body surface across species contain disproportionately large numbers of neurons dedicated to glabrous skin sensation, in part reflecting a higher density of mechanoreceptors that innervate these skin regions. Here, we find that disproportionate representation of glabrous skin emerges over postnatal development at the first synapse between peripheral mechanoreceptors and their central targets in the brainstem. Mechanoreceptor synapses undergo developmental refinement that depends on proximity of their terminals to glabrous skin, such that those innervating glabrous skin make synaptic connections that expand their central representation. In mice incapable of sensing gentle touch, mechanoreceptors innervating glabrous skin still make more powerful synapses in the brainstem. We propose that the skin region a mechanoreceptor innervates controls the developmental refinement of its central synapses to shape the representation of touch in the brain.

Highlights

Perception relies on populations of sensory neurons that represent salient features of the physical world
Disproportionate expansion of glabrous skin representation emerges over postnatal development, while receptor density in the skin remains stable We investigated the development of glabrous skin representation in mouse S1
Recordings from hindpaw regions of postnatal day 14 (P14) cortex showed an equal number of S1 neurons responding to paw glabrous and paw hairy skin stroke, while forepaw cortex emphasized paw glabrous skin surfaces (Figures 1B and 1C)

Summary

Introduction

Perception relies on populations of sensory neurons that represent salient features of the physical world. Neurons are not uniformly allocated across a sensory space, but rather, particular regions are often represented by disproportionate numbers of neurons. A striking example is the primate visual system, where neurons across the visual hierarchy disproportionately represent central regions of the visual field, in part reflecting the high density of photoreceptors in the center of the primate retina (Cowey and Rolls, 1974). Disproportionate central representation of foveal visual space has far-reaching consequences, as it shapes the ocular motor strategies used to survey the world as well as cognitive strategies used to comprehend visual scenes (Yarbus, 1967). The human somatosensory cortex contains an iconic map of the body, the homunculus, that does not faithfully reflect our physical form but rather disproportionately allocates neurons to the hands and face relative to the torso and proximal limbs (Penfield and Boldrey, 1937). Disproportionate central representation may reflect the tension between completely tiling a sensory space and allocating neural resources to areas where acuity or representational capacity is critical

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