Developmental 'awakening' of primary motor cortex to the sensory consequences of movement.

James C Dooley,Mark S Blumberg

doi:10.7554/elife.41841

Abstract

Before primary motor cortex (M1) develops its motor functions, it functions like a somatosensory area. Here, by recording from neurons in the forelimb representation of M1 in postnatal day (P) 8-12 rats, we demonstrate a rapid shift in its sensory responses. At P8-10, M1 neurons respond overwhelmingly to feedback from sleep-related twitches of the forelimb, but the same neurons do not respond to wake-related movements. By P12, M1 neurons suddenly respond to wake movements, a transition that results from opening the sensory gate in the external cuneate nucleus. Also at P12, fewer M1 neurons respond to individual twitches, but the full complement of twitch-related feedback observed at P8 is unmasked through local disinhibition. Finally, through P12, M1 sensory responses originate in the deep thalamorecipient layers, not primary somatosensory cortex. These findings demonstrate that M1 initially establishes a sensory framework upon which its later-emerging role in motor control is built.

Highlights

In placental mammals, primary motor cortex (M1) plays a critical role in adapting behavior to an ever-changing environment (Kawai et al, 2015)
One possibility is that M1 first develops a sensory framework, and it is upon this framework that its later-emerging motor functions rest (Bruce and Tatton, 1980; Chakrabarty and Martin, 2005)
The present findings strongly support the idea that M1 is built on a sensory framework that scaffolds its later-emerging motor map (Chakrabarty and Martin, 2005; Huntley, 1997b; Keller et al, 1996)

Summary

Introduction

Primary motor cortex (M1) plays a critical role in adapting behavior to an ever-changing environment (Kawai et al, 2015). In rats, intracortical microstimulation of M1 neurons does not evoke movements until postnatal day (P) 35 (Young et al, 2012). It is not understood why M1 shows such protracted development or how M1 functions before it assumes its ‘motor identity.’. Beginning early in development in rats, M1 neurons respond to externally generated (i.e. exafferent) stimulation (An et al, 2014; Asanuma, 1981; Tiriac and Blumberg, 2016).

Methods

Discussion

Conclusion