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Releasing dentate nucleus cells from Purkinje cell inhibition generates output from the cerebrocerebellum

Ishikawa, T and Tomatsu, S and Tsunoda, Y and Lee, J and Hoffman, DS and Kakei, S (2014) Releasing dentate nucleus cells from Purkinje cell inhibition generates output from the cerebrocerebellum. PLoS ONE, 9 (10).

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Abstract

© 2014 Ishikawa et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The cerebellum generates its vast amount of output to the cerebral cortex through the dentate nucleus (DN) that is essential for precise limb movements in primates. Nuclear cells in DN generate burst activity prior to limb movement, and inactivation of DN results in cerebellar ataxia. The question is how DN cells become active under intensive inhibitory drive from Purkinje cells (PCs). There are two excitatory inputs to DN, mossy fiber and climbing fiber collaterals, but neither of them appears to have sufficient strength for generation of burst activity in DN. Therefore, we can assume two possible mechanisms: post-inhibitory rebound excitation and disinhibition. If rebound excitation works, phasic excitation of PCs and a concomitant inhibition of DN cells should precede the excitation of DN cells. On the other hand, if disinhibition plays a primary role, phasic suppression of PCs and activation of DN cells should be observed at the same timing. To examine these two hypotheses, we compared the activity patterns of PCs in the cerebrocerebellum and DN cells during step-tracking wrist movements in three Japanese monkeys. As a result, we found that the majority of wrist-movement-related PCs were suppressed prior to movement onset and the majority of wrist-movement-related DN cells showed concurrent burst activity without prior suppression. In a minority of PCs and DN cells, movement-related increases and decreases in activity, respectively, developed later. These activity patterns suggest that the initial burst activity in DN cells is generated by reduced inhibition from PCs, i.e., by disinhibition. Our results indicate that suppression of PCs, which has been considered secondary to facilitation, plays the primary role in generating outputs from DN. Our findings provide a new perspective on the mechanisms used by PCs to influence limb motor control and on the plastic changes that underlie motor learning in the cerebrocerebellum.


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Details

Item Type: Article
Status: Published
Creators/Authors:
CreatorsEmailPitt UsernameORCID
Ishikawa, T
Tomatsu, S
Tsunoda, Y
Lee, J
Hoffman, DS
Kakei, S
Contributors:
ContributionContributors NameEmailPitt UsernameORCID
EditorAumann, Tim D.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Centers: Other Centers, Institutes, Offices, or Units > Center for the Neural Basis of Cognition
Date: 1 October 2014
Date Type: Publication
Journal or Publication Title: PLoS ONE
Volume: 9
Number: 10
DOI or Unique Handle: 10.1371/journal.pone.0108774
Schools and Programs: School of Medicine > Neurobiology
Refereed: Yes
Other ID: NLM PMC4184834
PubMed Central ID: PMC4184834
PubMed ID: 25279763
Date Deposited: 12 May 2015 18:00
Last Modified: 13 Oct 2017 22:57
URI: http://d-scholarship.pitt.edu/id/eprint/24026

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