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, though self-generated, trigger abundant reafferent activation of sensorimotor circuits in the developing brain.
Article and author information
Author details
Funding
National Institutes of Health (R37-HD081168)
- Mark S Blumberg
National Institutes of Health (R01-HD063071)
- Mark S Blumberg
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- David Kleinfeld, University of California, San Diego, United States
Ethics
Animal experimentation: All experiments were carried out in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals (NIH Publication No. 80-23) and were approved by the Institutional Animal Care and Use Committee of the University of Iowa (protocol numbers 1202054 and 1403038).
Version history
- Received: June 13, 2016
- Accepted: July 29, 2016
- Accepted Manuscript published: August 3, 2016 (version 1)
- Version of Record published: August 23, 2016 (version 2)
Copyright
© 2016, Tiriac & Blumberg
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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