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Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements

Clues from human movement disorders have long suggested that the neurotransmitter dopamine plays a role in motor control, but how the endogenous dopaminergic system influences movement is unknown. Here, we examined the relationship between dopaminergic signaling and the timing of reward-related move...

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Autores principales: Hamilos, Allison E, Spedicato, Giulia, Hong, Ye, Sun, Fangmiao, Li, Yulong, Assad, John A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8860451/
https://www.ncbi.nlm.nih.gov/pubmed/34939925
http://dx.doi.org/10.7554/eLife.62583
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author Hamilos, Allison E
Spedicato, Giulia
Hong, Ye
Sun, Fangmiao
Li, Yulong
Assad, John A
author_facet Hamilos, Allison E
Spedicato, Giulia
Hong, Ye
Sun, Fangmiao
Li, Yulong
Assad, John A
author_sort Hamilos, Allison E
collection PubMed
description Clues from human movement disorders have long suggested that the neurotransmitter dopamine plays a role in motor control, but how the endogenous dopaminergic system influences movement is unknown. Here, we examined the relationship between dopaminergic signaling and the timing of reward-related movements in mice. Animals were trained to initiate licking after a self-timed interval following a start-timing cue; reward was delivered in response to movements initiated after a criterion time. The movement time was variable from trial-to-trial, as expected from previous studies. Surprisingly, dopaminergic signals ramped-up over seconds between the start-timing cue and the self-timed movement, with variable dynamics that predicted the movement/reward time on single trials. Steeply rising signals preceded early lick-initiation, whereas slowly rising signals preceded later initiation. Higher baseline signals also predicted earlier self-timed movements. Optogenetic activation of dopamine neurons during self-timing did not trigger immediate movements, but rather caused systematic early-shifting of movement initiation, whereas inhibition caused late-shifting, as if modulating the probability of movement. Consistent with this view, the dynamics of the endogenous dopaminergic signals quantitatively predicted the moment-by-moment probability of movement initiation on single trials. We propose that ramping dopaminergic signals, likely encoding dynamic reward expectation, can modulate the decision of when to move.
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spelling pubmed-88604512022-02-23 Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements Hamilos, Allison E Spedicato, Giulia Hong, Ye Sun, Fangmiao Li, Yulong Assad, John A eLife Neuroscience Clues from human movement disorders have long suggested that the neurotransmitter dopamine plays a role in motor control, but how the endogenous dopaminergic system influences movement is unknown. Here, we examined the relationship between dopaminergic signaling and the timing of reward-related movements in mice. Animals were trained to initiate licking after a self-timed interval following a start-timing cue; reward was delivered in response to movements initiated after a criterion time. The movement time was variable from trial-to-trial, as expected from previous studies. Surprisingly, dopaminergic signals ramped-up over seconds between the start-timing cue and the self-timed movement, with variable dynamics that predicted the movement/reward time on single trials. Steeply rising signals preceded early lick-initiation, whereas slowly rising signals preceded later initiation. Higher baseline signals also predicted earlier self-timed movements. Optogenetic activation of dopamine neurons during self-timing did not trigger immediate movements, but rather caused systematic early-shifting of movement initiation, whereas inhibition caused late-shifting, as if modulating the probability of movement. Consistent with this view, the dynamics of the endogenous dopaminergic signals quantitatively predicted the moment-by-moment probability of movement initiation on single trials. We propose that ramping dopaminergic signals, likely encoding dynamic reward expectation, can modulate the decision of when to move. eLife Sciences Publications, Ltd 2021-12-23 /pmc/articles/PMC8860451/ /pubmed/34939925 http://dx.doi.org/10.7554/eLife.62583 Text en © 2021, Hamilos et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Hamilos, Allison E
Spedicato, Giulia
Hong, Ye
Sun, Fangmiao
Li, Yulong
Assad, John A
Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements
title Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements
title_full Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements
title_fullStr Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements
title_full_unstemmed Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements
title_short Slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements
title_sort slowly evolving dopaminergic activity modulates the moment-to-moment probability of reward-related self-timed movements
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8860451/
https://www.ncbi.nlm.nih.gov/pubmed/34939925
http://dx.doi.org/10.7554/eLife.62583
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