Abstract

Before primary motor cortex (M1) develops its motor functions, it behaves 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 change in the types of movements that trigger sensory responses. At P8-10, M1 neurons respond overwhelmingly to sleep-related twitches of the forelimb, but the same neurons do not respond to forelimb movements when the animal is awake. Then, only two days later, M1 neurons suddenly respond to feedback from wake movements; this transition results from a change in sensory gating by the external cuneate nucleus. Also, at P12, the onset of local cortical inhibition leads to fewer M1 neurons responding to twitches; pharmacological disinhibition unmasks the more robust twitch responsiveness observed at P8. Thus, M1 initially establishes a somatosensory framework that lays a foundation for later-emerging motor control and plasticity.

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)

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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).

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