Spatiotemporal reorganization of corticostriatal networks encodes motor skill learning
Summary: Motor skill learning requires the activity of the dorsal striatum, with a differential global implication of the dorsomedial and dorsolateral territories. We investigate here whether and how specific striatal neurons encode the acquisition and consolidation of a motor skill. Using ex vivo t...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-04-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124722003710 |
| _version_ | 1819047296170459136 |
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| author | Nagham Badreddine Gisela Zalcman Florence Appaix Guillaume Becq Nicolas Tremblay Frédéric Saudou Sophie Achard Elodie Fino |
| author_facet | Nagham Badreddine Gisela Zalcman Florence Appaix Guillaume Becq Nicolas Tremblay Frédéric Saudou Sophie Achard Elodie Fino |
| author_sort | Nagham Badreddine |
| collection | DOAJ |
| description | Summary: Motor skill learning requires the activity of the dorsal striatum, with a differential global implication of the dorsomedial and dorsolateral territories. We investigate here whether and how specific striatal neurons encode the acquisition and consolidation of a motor skill. Using ex vivo two-photon calcium imaging after rotarod training, we report that highly active (HA) striatal populations arise from distinct spatiotemporal reorganization in the dorsomedial (DMS) and dorsolateral (DLS) striatum networks and are correlated with learning performance. The DMS overall activity decreases in early training, with few and sparsely distributed HA cells, while the DLS shows a progressive and long-lasting formation of HA cell clusters. These reorganizations result from reinforcement of synaptic connections to the DMS and anatomical rearrangements to the DLS. Targeted silencing of DMS or DLS HA cells with the cFos-TRAP strategy strongly impairs individual performance. Our data reveal that discrete domains of striatal populations encode acquisition and long-lasting retention of a motor skill. |
| first_indexed | 2024-12-21T10:58:06Z |
| format | Article |
| id | doaj.art-5797c3684a8b494e80e6cadbcd903fd0 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-12-21T10:58:06Z |
| publishDate | 2022-04-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-5797c3684a8b494e80e6cadbcd903fd02022-12-21T19:06:26ZengElsevierCell Reports2211-12472022-04-01391110623Spatiotemporal reorganization of corticostriatal networks encodes motor skill learningNagham Badreddine0Gisela Zalcman1Florence Appaix2Guillaume Becq3Nicolas Tremblay4Frédéric Saudou5Sophie Achard6Elodie Fino7Université Grenoble Alpes, INSERM, U1216, CHU Grenoble Alpes, CNRS, Grenoble Institut Neurosciences, 38000 Grenoble, FranceUniversité Grenoble Alpes, INSERM, U1216, CHU Grenoble Alpes, CNRS, Grenoble Institut Neurosciences, 38000 Grenoble, FranceUniversité Grenoble Alpes, INSERM, U1216, CHU Grenoble Alpes, CNRS, Grenoble Institut Neurosciences, 38000 Grenoble, FranceUniversité Grenoble Alpes, CNRS, Grenoble INP, GIPSA-Lab, 38000 Grenoble, FranceUniversité Grenoble Alpes, CNRS, Grenoble INP, GIPSA-Lab, 38000 Grenoble, FranceUniversité Grenoble Alpes, INSERM, U1216, CHU Grenoble Alpes, CNRS, Grenoble Institut Neurosciences, 38000 Grenoble, FranceUniversité Grenoble Alpes, Inria, CNRS, Grenoble INP, LJK, 38000 Grenoble, FranceUniversité Grenoble Alpes, INSERM, U1216, CHU Grenoble Alpes, CNRS, Grenoble Institut Neurosciences, 38000 Grenoble, France; Corresponding authorSummary: Motor skill learning requires the activity of the dorsal striatum, with a differential global implication of the dorsomedial and dorsolateral territories. We investigate here whether and how specific striatal neurons encode the acquisition and consolidation of a motor skill. Using ex vivo two-photon calcium imaging after rotarod training, we report that highly active (HA) striatal populations arise from distinct spatiotemporal reorganization in the dorsomedial (DMS) and dorsolateral (DLS) striatum networks and are correlated with learning performance. The DMS overall activity decreases in early training, with few and sparsely distributed HA cells, while the DLS shows a progressive and long-lasting formation of HA cell clusters. These reorganizations result from reinforcement of synaptic connections to the DMS and anatomical rearrangements to the DLS. Targeted silencing of DMS or DLS HA cells with the cFos-TRAP strategy strongly impairs individual performance. Our data reveal that discrete domains of striatal populations encode acquisition and long-lasting retention of a motor skill.http://www.sciencedirect.com/science/article/pii/S2211124722003710CP: Neuroscience |
| spellingShingle | Nagham Badreddine Gisela Zalcman Florence Appaix Guillaume Becq Nicolas Tremblay Frédéric Saudou Sophie Achard Elodie Fino Spatiotemporal reorganization of corticostriatal networks encodes motor skill learning Cell Reports CP: Neuroscience |
| title | Spatiotemporal reorganization of corticostriatal networks encodes motor skill learning |
| title_full | Spatiotemporal reorganization of corticostriatal networks encodes motor skill learning |
| title_fullStr | Spatiotemporal reorganization of corticostriatal networks encodes motor skill learning |
| title_full_unstemmed | Spatiotemporal reorganization of corticostriatal networks encodes motor skill learning |
| title_short | Spatiotemporal reorganization of corticostriatal networks encodes motor skill learning |
| title_sort | spatiotemporal reorganization of corticostriatal networks encodes motor skill learning |
| topic | CP: Neuroscience |
| url | http://www.sciencedirect.com/science/article/pii/S2211124722003710 |
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