Coupling between motor cortex and striatum increases during sleep over long-term skill learning
The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknow...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/64303 |
| _version_ | 1811228042352132096 |
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| author | Stefan M Lemke Dhakshin S Ramanathan David Darevksy Daniel Egert Joshua D Berke Karunesh Ganguly |
| author_facet | Stefan M Lemke Dhakshin S Ramanathan David Darevksy Daniel Egert Joshua D Berke Karunesh Ganguly |
| author_sort | Stefan M Lemke |
| collection | DOAJ |
| description | The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or ‘offline’ during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-rapid-eye-movement (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements, and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning. |
| first_indexed | 2024-04-12T09:51:50Z |
| format | Article |
| id | doaj.art-25268be2faeb47068dab872d32f76d1a |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T09:51:50Z |
| publishDate | 2021-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-25268be2faeb47068dab872d32f76d1a2022-12-22T03:37:49ZengeLife Sciences Publications LtdeLife2050-084X2021-09-011010.7554/eLife.64303Coupling between motor cortex and striatum increases during sleep over long-term skill learningStefan M Lemke0https://orcid.org/0000-0002-1721-5425Dhakshin S Ramanathan1David Darevksy2Daniel Egert3Joshua D Berke4https://orcid.org/0000-0003-1436-6823Karunesh Ganguly5https://orcid.org/0000-0002-2570-9943Neuroscience Graduate Program, University of California, San Francisco, San Francisco, United States; Neurology Service, San Francisco Veterans Affairs Medical Center, San Francisco, United States; Department of Neurology, University of California, San Francisco, San Francisco, United States; Istituto Italiano di Tecnologia, Rovereto, ItalyDepartment of Psychiatry, University of California, San Diego, San Diego, United StatesNeurology Service, San Francisco Veterans Affairs Medical Center, San Francisco, United States; Department of Neurology, University of California, San Francisco, San Francisco, United StatesDepartment of Neurology, University of California, San Francisco, San Francisco, United StatesDepartment of Neurology, University of California, San Francisco, San Francisco, United States; Weill Institute for Neurosciences and Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, United StatesNeurology Service, San Francisco Veterans Affairs Medical Center, San Francisco, United States; Department of Neurology, University of California, San Francisco, San Francisco, United States; Weill Institute for Neurosciences and Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, United StatesThe strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or ‘offline’ during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-rapid-eye-movement (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements, and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning.https://elifesciences.org/articles/64303sleepspindlereactivationlocal field potentiallearningmotor cortex |
| spellingShingle | Stefan M Lemke Dhakshin S Ramanathan David Darevksy Daniel Egert Joshua D Berke Karunesh Ganguly Coupling between motor cortex and striatum increases during sleep over long-term skill learning eLife sleep spindle reactivation local field potential learning motor cortex |
| title | Coupling between motor cortex and striatum increases during sleep over long-term skill learning |
| title_full | Coupling between motor cortex and striatum increases during sleep over long-term skill learning |
| title_fullStr | Coupling between motor cortex and striatum increases during sleep over long-term skill learning |
| title_full_unstemmed | Coupling between motor cortex and striatum increases during sleep over long-term skill learning |
| title_short | Coupling between motor cortex and striatum increases during sleep over long-term skill learning |
| title_sort | coupling between motor cortex and striatum increases during sleep over long term skill learning |
| topic | sleep spindle reactivation local field potential learning motor cortex |
| url | https://elifesciences.org/articles/64303 |
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