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Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety

Anxiety results in sub-optimal motor learning, but the precise mechanisms through which this effect occurs remain unknown. Using a motor sequence learning paradigm with separate phases for initial exploration and reward-based learning, we show that anxiety states in humans impair learning by attenua...

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Detalles Bibliográficos
Autores principales: Sporn, Sebastian, Hein, Thomas, Herrojo Ruiz, Maria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7237220/
https://www.ncbi.nlm.nih.gov/pubmed/32423530
http://dx.doi.org/10.7554/eLife.50654
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author Sporn, Sebastian
Hein, Thomas
Herrojo Ruiz, Maria
author_facet Sporn, Sebastian
Hein, Thomas
Herrojo Ruiz, Maria
author_sort Sporn, Sebastian
collection PubMed
description Anxiety results in sub-optimal motor learning, but the precise mechanisms through which this effect occurs remain unknown. Using a motor sequence learning paradigm with separate phases for initial exploration and reward-based learning, we show that anxiety states in humans impair learning by attenuating the update of reward estimates. Further, when such estimates are perceived as unstable over time (volatility), anxiety constrains adaptive behavioral changes. Neurally, anxiety during initial exploration increased the amplitude and the rate of long bursts of sensorimotor and prefrontal beta oscillations (13–30 Hz). These changes extended to the subsequent learning phase, where phasic increases in beta power and burst rate following reward feedback were linked to smaller updates in reward estimates, with a higher anxiety-related increase explaining the attenuated belief updating. These data suggest that state anxiety alters the dynamics of beta oscillations during reward processing, thereby impairing proper updating of motor predictions when learning in unstable environments.
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spelling pubmed-72372202020-05-20 Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety Sporn, Sebastian Hein, Thomas Herrojo Ruiz, Maria eLife Neuroscience Anxiety results in sub-optimal motor learning, but the precise mechanisms through which this effect occurs remain unknown. Using a motor sequence learning paradigm with separate phases for initial exploration and reward-based learning, we show that anxiety states in humans impair learning by attenuating the update of reward estimates. Further, when such estimates are perceived as unstable over time (volatility), anxiety constrains adaptive behavioral changes. Neurally, anxiety during initial exploration increased the amplitude and the rate of long bursts of sensorimotor and prefrontal beta oscillations (13–30 Hz). These changes extended to the subsequent learning phase, where phasic increases in beta power and burst rate following reward feedback were linked to smaller updates in reward estimates, with a higher anxiety-related increase explaining the attenuated belief updating. These data suggest that state anxiety alters the dynamics of beta oscillations during reward processing, thereby impairing proper updating of motor predictions when learning in unstable environments. eLife Sciences Publications, Ltd 2020-05-19 /pmc/articles/PMC7237220/ /pubmed/32423530 http://dx.doi.org/10.7554/eLife.50654 Text en © 2020, Sporn et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Sporn, Sebastian
Hein, Thomas
Herrojo Ruiz, Maria
Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety
title Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety
title_full Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety
title_fullStr Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety
title_full_unstemmed Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety
title_short Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety
title_sort alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7237220/
https://www.ncbi.nlm.nih.gov/pubmed/32423530
http://dx.doi.org/10.7554/eLife.50654
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