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Cerebellar-Recipient Motor Thalamus Drives Behavioral Context-Specific Movement Initiation

41 Pages Posted: 18 Oct 2019 Sneak Peek Status: Review Complete

See all articles by Joshua Dacre

Joshua Dacre

University of Edinburgh - Centre for Discovery Brain Sciences

Matt Colligan

University of Edinburgh - Centre for Discovery Brain Sciences

Julian Ammer

University of Edinburgh - Centre for Discovery Brain Sciences

Julia Schiemann

University of Edinburgh - Centre for Discovery Brain Sciences

Thomas Clarke

University of Edinburgh - Centre for Discovery Brain Sciences

Victor Chamosa-Pino

University of Edinburgh - Centre for Discovery Brain Sciences

Federico Claudi

University of Edinburgh - Centre for Discovery Brain Sciences

J. Alex Harston

University of Edinburgh - Centre for Discovery Brain Sciences

Constantinos Eleftheriou

University of Edinburgh - Centre for Discovery Brain Sciences

Janelle Pakan

University of Edinburgh - Centre for Discovery Brain Sciences

Cheng-Chiu Huang

Howard Hughes Medical Institute (HHMI) - Chevy Chase - Janelia Research Campus

Adam Hantman

Howard Hughes Medical Institute (HHMI) - Chevy Chase - Janelia Research Campus

Nathalie Rochefort

University of Edinburgh - Centre for Discovery Brain Sciences

Ian Duguid

University of Edinburgh - Centre for Discovery Brain Sciences

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Abstract

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.

Keywords: Motor behavior, cerebellar thalamocortical pathway, movement initiation, goal-directed, motor timing signal, photostimulation, in vivo patch-clamp electrophysiology, GRIN lens-mediated population calcium imaging, forelimb kinematics, cued forelimb push task

Suggested Citation

Dacre, Joshua and Colligan, Matt and Ammer, Julian and Schiemann, Julia and Clarke, Thomas and Chamosa-Pino, Victor and Claudi, Federico and Harston, J. Alex and Eleftheriou, Constantinos and Pakan, Janelle and Huang, Cheng-Chiu and Hantman, Adam and Rochefort, Nathalie and Duguid, Ian, Cerebellar-Recipient Motor Thalamus Drives Behavioral Context-Specific Movement Initiation (October 15, 2019). Available at SSRN: https://ssrn.com/abstract=3470398 or http://dx.doi.org/10.2139/ssrn.3470398
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Joshua Dacre

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Matt Colligan

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Julian Ammer

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Julia Schiemann

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Thomas Clarke

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Victor Chamosa-Pino

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Federico Claudi

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

J. Alex Harston

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Constantinos Eleftheriou

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Janelle Pakan

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Cheng-Chiu Huang

Howard Hughes Medical Institute (HHMI) - Chevy Chase - Janelia Research Campus

19700 Helix Drive
Ashburn, VA 20147
United States

Adam Hantman

Howard Hughes Medical Institute (HHMI) - Chevy Chase - Janelia Research Campus

19700 Helix Drive
Ashburn, VA 20147
United States

Nathalie Rochefort

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

Ian Duguid (Contact Author)

University of Edinburgh - Centre for Discovery Brain Sciences

Old College
South Bridge
Edinburgh, Scotland EH8 9JY
United Kingdom

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