Precisely timed dopamine signals establish distinct kinematic representations of skilled movements
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 functio...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2020-11-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/61591 |
_version_ | 1811252889253838848 |
---|---|
author | Alexandra Bova Matt Gaidica Amy Hurst Yoshiko Iwai Julia Hunter Daniel K Leventhal |
author_facet | Alexandra Bova Matt Gaidica Amy Hurst Yoshiko Iwai Julia Hunter Daniel K Leventhal |
author_sort | Alexandra Bova |
collection | DOAJ |
description | 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. |
first_indexed | 2024-04-12T16:42:20Z |
format | Article |
id | doaj.art-63645294306d449c9a6c4cdd7a154957 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-12T16:42:20Z |
publishDate | 2020-11-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
spelling | doaj.art-63645294306d449c9a6c4cdd7a1549572022-12-22T03:24:44ZengeLife Sciences Publications LtdeLife2050-084X2020-11-01910.7554/eLife.61591Precisely timed dopamine signals establish distinct kinematic representations of skilled movementsAlexandra Bova0Matt Gaidica1https://orcid.org/0000-0002-0191-1899Amy Hurst2Yoshiko Iwai3Julia Hunter4Daniel K Leventhal5https://orcid.org/0000-0001-8174-5933Neuroscience Graduate Program, University of Michigan, Ann Arbor, United StatesNeuroscience Graduate Program, University of Michigan, Ann Arbor, United StatesDepartment of Neurology, University of Michigan, Ann Arbor, United StatesDepartment of Neurology, University of Michigan, Ann Arbor, United StatesDepartment of Neurology, University of Michigan, Ann Arbor, United StatesDepartment of Neurology, University of Michigan, Ann Arbor, United States; Department of Biomedical Engineering, University of Michigan, Ann Arbor, United States; Parkinson Disease Foundation Research Center of Excellence, University of Michigan, Ann Arbor, United States; Department of Neurology, VA Ann Arbor Health System, Ann Arbor, United StatesBrain 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.https://elifesciences.org/articles/61591dopaminedexterous skillmotion trackingskilled reachingkinematics |
spellingShingle | Alexandra Bova Matt Gaidica Amy Hurst Yoshiko Iwai Julia Hunter Daniel K Leventhal Precisely timed dopamine signals establish distinct kinematic representations of skilled movements eLife dopamine dexterous skill motion tracking skilled reaching kinematics |
title | Precisely timed dopamine signals establish distinct kinematic representations of skilled movements |
title_full | Precisely timed dopamine signals establish distinct kinematic representations of skilled movements |
title_fullStr | Precisely timed dopamine signals establish distinct kinematic representations of skilled movements |
title_full_unstemmed | Precisely timed dopamine signals establish distinct kinematic representations of skilled movements |
title_short | Precisely timed dopamine signals establish distinct kinematic representations of skilled movements |
title_sort | precisely timed dopamine signals establish distinct kinematic representations of skilled movements |
topic | dopamine dexterous skill motion tracking skilled reaching kinematics |
url | https://elifesciences.org/articles/61591 |
work_keys_str_mv | AT alexandrabova preciselytimeddopaminesignalsestablishdistinctkinematicrepresentationsofskilledmovements AT mattgaidica preciselytimeddopaminesignalsestablishdistinctkinematicrepresentationsofskilledmovements AT amyhurst preciselytimeddopaminesignalsestablishdistinctkinematicrepresentationsofskilledmovements AT yoshikoiwai preciselytimeddopaminesignalsestablishdistinctkinematicrepresentationsofskilledmovements AT juliahunter preciselytimeddopaminesignalsestablishdistinctkinematicrepresentationsofskilledmovements AT danielkleventhal preciselytimeddopaminesignalsestablishdistinctkinematicrepresentationsofskilledmovements |