Self-Generated Movements with “Unexpected” Sensory Consequences

The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals g...

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Bibliographic Details
Published in:Current biology 2014-09, Vol.24 (18), p.2136-2141
Main Authors: Tiriac, Alexandre, Del Rio-Bermudez, Carlos, Blumberg, Mark S.
Format: Article
Language:English
Subjects:
Animals
Female
Male
Motor Cortex - physiology
Movement
Proprioception
Rats
Rats, Sprague-Dawley
Signal Transduction
Sleep, REM
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Summary:The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1–3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6–10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep—a behavioral state that predominates in early infancy [12–16]—neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20–23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21–23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected. •Reafference from REM sleep twitches, but not wake movements, triggers M1 activity•Only “unexpected” self-generated movements trigger M1 activity•Twitches are processed as if they are unexpected It is generally assumed that all self-generated movements are accompanied by motor copies that help animals distinguish expected from unexpected sensory input. Here, in newborn rats, Tiriac et al. provide evidence for self-generated movements that are processed as if they are unexpected. Remarkably, these movements occur during REM sleep.
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2014.07.053