Letter | Published:

Opponent and bidirectional control of movement velocity in the basal ganglia

Nature volume 533, pages 402406 (19 May 2016) | Download Citation

Abstract

For goal-directed behaviour it is critical that we can both select the appropriate action and learn to modify the underlying movements (for example, the pitch of a note or velocity of a reach) to improve outcomes. The basal ganglia are a critical nexus where circuits necessary for the production of behaviour, such as the neocortex and thalamus, are integrated with reward signalling1 to reinforce successful, purposive actions2. The dorsal striatum, a major input structure of basal ganglia, is composed of two opponent pathways, direct and indirect, thought to select actions that elicit positive outcomes and suppress actions that do not, respectively3,4. Activity-dependent plasticity modulated by reward is thought to be sufficient for selecting actions in the striatum5,6. Although perturbations of basal ganglia function produce profound changes in movement7, it remains unknown whether activity-dependent plasticity is sufficient to produce learned changes in movement kinematics, such as velocity. Here we use cell-type-specific stimulation in mice delivered in closed loop during movement to demonstrate that activity in either the direct or indirect pathway is sufficient to produce specific and sustained increases or decreases in velocity, without affecting action selection or motivation. These behavioural changes were a form of learning that accumulated over trials, persisted after the cessation of stimulation, and were abolished in the presence of dopamine antagonists. Our results reveal that the direct and indirect pathways can each bidirectionally control movement velocity, demonstrating unprecedented specificity and flexibility in the control of volition by the basal ganglia.

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Acknowledgements

This work was supported by funding from the Howard Hughes Medical Institute. J.T.D. is a Group Leader at Janelia Research Campus. We thank A. Lee, A. Karpova, N. Spruston, and members of our laboratory for critical reading and feedback on the manuscript. We also thank M. Frank for helpful discussions of the OpAL model.

Author information

Affiliations

  1. Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, Virginia 20147, USA

    • Eric A. Yttri
    •  & Joshua T. Dudman

Authors

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Contributions

E.A.Y. performed the experiments and analysed the data. E.A.Y. and J.T.D. designed the experiments, performed the modelling, and wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Joshua T. Dudman.

Extended data

Supplementary information

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    Supplementary Information

    This file contains a Supplementary Discussion and additional references.

Videos

  1. 1.

    dMSN upper third stimulation

    Infrared video recording of a Drd1a-cre::Ai32 mouse performing task while head-fixed during stimulation session for upper 1/3 stimulation protocols. Black line indicates eccentricity. Green line indicates outward velocity. Blue bar indicates period of stimulation. Video angle may cause joystick to appear closer to mouse platform than it is (2.7cm away).

  2. 2.

    iMSN upper third stimulation

    Infrared video recording of a Drd2-cre::Ai32 mouse performing task while head-fixed during stimulation session for upper 1/3 stimulation protocols. Black line indicates eccentricity. Green line indicates outward velocity. Blue bar indicates period of stimulation.

  3. 3.

    dMSN lower third stimulation

    Infrared video recording of a Drd1a-cre::Ai32 mouse performing task while head-fixed during stimulation session for lower 1/3 stimulation protocols. Black line indicates eccentricity. Green line indicates outward velocity. Blue bar indicates period of stimulation.

  4. 4.

    iMSN lower third stimulation

    Infrared video recording of a Drd2-cre::Ai32 mouse performing task while head-fixed during stimulation session for lower 1/3 stimulation protocols. Black line indicates eccentricity. Green line indicates outward velocity. Blue bar indicates period of stimulation.

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DOI

https://doi.org/10.1038/nature17639

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