Gating of reafference in the external cuneate nucleus during self-generated movements in wake but not sleep

Abstract

Nervous systems distinguish between self- and other-generated movements by monitoring discrepancies between planned and performed actions. To do so, corollary discharges are conveyed to sensory areas and gate expected reafference. Such gating is observed in neonatal rats during wake-related movements. In contrast, twitches, which are self-generated movements produced during active (or REM) sleep, differ from wake movements in that they reliably trigger robust neural activity. Accordingly, we hypothesized that the gating actions of corollary discharge are absent during twitching. Here, we identify the external cuneate nucleus (ECN), which processes sensory input from the forelimbs, as a site of movement-dependent sensory gating during wake. Whereas pharmacological disinhibition of the ECN unmasked wake-related reafference, twitch-related reafference was unaffected. This is the first demonstration of a neural comparator that is differentially engaged depending on the kind of movement produced. This mechanism explains how twitches, although self-generated, trigger abundant reafferent activation of sensorimotor circuits in the developing brain.