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Cerebellar-recipient motor thalamus drives behavioral context-specific movement initiation

View ORCID ProfileJoshua Dacre, Matt Colligan, Julian Ammer, Julia Schiemann, View ORCID ProfileThomas Clarke, View ORCID ProfileVictor Chamosa-Pino, View ORCID ProfileFederico Claudi, View ORCID ProfileJ. Alex Harston, View ORCID ProfileConstantinos Eleftheriou, View ORCID ProfileJanelle M.P. Pakan, Cheng-Chiu Huang, View ORCID ProfileAdam Hantman, View ORCID ProfileNathalie L. Rochefort, View ORCID ProfileIan Duguid
doi: https://doi.org/10.1101/802124
Joshua Dacre
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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  • For correspondence: jdacre@ed.ac.uk Ian.Duguid@ed.ac.uk
Matt Colligan
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Julian Ammer
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Julia Schiemann
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Thomas Clarke
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Victor Chamosa-Pino
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Federico Claudi
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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J. Alex Harston
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Constantinos Eleftheriou
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Janelle M.P. Pakan
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Cheng-Chiu Huang
3Janelia Research Campus, HHMI, Ashburn, Virginia, 20147, USA
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Adam Hantman
3Janelia Research Campus, HHMI, Ashburn, Virginia, 20147, USA
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Nathalie L. Rochefort
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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Ian Duguid
1Centre for Discovery Brain Sciences and Patrick Wild Centre, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, Edinburgh, EH8 9XD, UK
2Simons Initiative for the Developing Brain, University of Edinburgh, Edinburgh, EH8 9XD, UK
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  • For correspondence: jdacre@ed.ac.uk Ian.Duguid@ed.ac.uk
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Summary

To initiate goal-directed behavior, animals must transform sensory cues into motor commands that generate appropriately timed actions. Sensorimotor transformations along the cerebellar-thalamocortical pathway are thought to shape motor cortical output and movement timing, but whether this pathway initiates goal-directed movement remains poorly understood. Here, we recorded and perturbed activity in cerebellar-recipient regions of motor thalamus (dentate / interpositus nucleus-recipient regions, MThDN/IPN) and primary motor cortex (M1) in mice trained to execute a cued forelimb lever push task for reward. MThDN/IPN population responses were dominated by a time-locked increase in activity immediately prior to movement that was temporally uncoupled from cue presentation, providing a fixed latency feedforward motor timing signal to M1FL. Blocking MThDN/IPN output suppressed cued movement initiation. Stimulating the MThDN/IPN thalamocortical pathway in the absence of the cue recapitulated cue-evoked M1 membrane potential dynamics and forelimb behavior in the learned behavioral context, but generated semi-random movements in an altered behavioral context. Thus, cerebellar-recipient motor thalamocortical input to M1 is indispensable for the generation of motor commands that initiate goal-directed movement, refining our understanding of how the cerebellar-thalamocortical pathway contributes to movement timing.

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Posted October 16, 2019.
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Cerebellar-recipient motor thalamus drives behavioral context-specific movement initiation
Joshua Dacre, Matt Colligan, Julian Ammer, Julia Schiemann, Thomas Clarke, Victor Chamosa-Pino, Federico Claudi, J. Alex Harston, Constantinos Eleftheriou, Janelle M.P. Pakan, Cheng-Chiu Huang, Adam Hantman, Nathalie L. Rochefort, Ian Duguid
bioRxiv 802124; doi: https://doi.org/10.1101/802124
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Cerebellar-recipient motor thalamus drives behavioral context-specific movement initiation
Joshua Dacre, Matt Colligan, Julian Ammer, Julia Schiemann, Thomas Clarke, Victor Chamosa-Pino, Federico Claudi, J. Alex Harston, Constantinos Eleftheriou, Janelle M.P. Pakan, Cheng-Chiu Huang, Adam Hantman, Nathalie L. Rochefort, Ian Duguid
bioRxiv 802124; doi: https://doi.org/10.1101/802124

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