Precisely-timed dopamine signals establish distinct kinematic representations of skilled movements

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Abstract

Brain dopamine is critical for normal motor control, as evidenced by its importance in Parkinson Disease and related disorders. Current hypotheses are that dopamine influences motor control by 'invigorating' movements and regulating motor learning. Most evidence for these aspects of dopamine function comes from simple tasks (e.g., lever pressing). Therefore, the influence of dopamine on motor skills requiring multi-joint coordination is unknown. To determine the effects of precisely-timed dopamine manipulations on the performance of a complex, finely coordinated dexterous skill, we optogenetically stimulated or inhibited midbrain dopamine neurons as rats performed a skilled reaching task. We found that reach kinematics and coordination between gross and fine movements progressively changed with repeated manipulations. However, once established, rats transitioned abruptly between aberrant and baseline reach kinematics in a dopamine-dependent manner. These results suggest that precisely-timed dopamine signals have immediate and long-term influences on motor skill performance, distinct from simply 'invigorating' movement.

Data availability

Original video files and extracted deeplabcut coordinates in .csv format are available publicly on Figshare in the Collection "Bova_Leventhal_2020 Precisely-timed dopamine signals establish distinct kinematic representations of skilled movements"

Article and author information

Author details

Alexandra Bova

Neuroscience Graduate Program, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Matt Gaidica

Neuroscience Graduate Program, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Amy Hurst

Neurology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Yoshiko Iwai

Neurology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Julia Hunter

Neurology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.
Daniel K Leventhal

Neurology, University of Michigan, Ann Arbor, United States

For correspondence
dleventh@med.umich.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8174-5933

Funding

National Institute of Neurological Disorders and Stroke (K08-NS072183)

Daniel K Leventhal

Nvidia (GPU grant)

Daniel K Leventhal

University of Michigan

Daniel K Leventhal

Brain Research Foundation (BRF Seed Grant)

Daniel K Leventhal

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to an approved institutional animal care and use committee (IACUC) protocol (#8407) of the University of Michigan. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Copyright

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.