Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus
Abstract Motor sequence learning (MSL) is supported by dynamical interactions between hippocampal and striatal networks that are thought to be orchestrated by the prefrontal cortex. In the present study, we tested whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal c...
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Nature Portfolio
2021-10-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-021-99926-1 |
| _version_ | 1819024853305393152 |
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| author | Mareike A. Gann Bradley R. King Nina Dolfen Menno P. Veldman Marco Davare Stephan P. Swinnen Dante Mantini Edwin M. Robertson Geneviève Albouy |
| author_facet | Mareike A. Gann Bradley R. King Nina Dolfen Menno P. Veldman Marco Davare Stephan P. Swinnen Dante Mantini Edwin M. Robertson Geneviève Albouy |
| author_sort | Mareike A. Gann |
| collection | DOAJ |
| description | Abstract Motor sequence learning (MSL) is supported by dynamical interactions between hippocampal and striatal networks that are thought to be orchestrated by the prefrontal cortex. In the present study, we tested whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex (DLPFC) prior to MSL can modulate multivoxel response patterns in the stimulated cortical area, the hippocampus and the striatum. Response patterns were assessed with multivoxel correlation structure analyses of functional magnetic resonance imaging data acquired during task practice and during resting-state scans before and after learning/stimulation. Results revealed that, across stimulation conditions, MSL induced greater modulation of task-related DLPFC multivoxel patterns than random practice. A similar learning-related modulatory effect was observed on sensorimotor putamen patterns under inhibitory stimulation. Furthermore, MSL as well as inhibitory stimulation affected (posterior) hippocampal multivoxel patterns at post-intervention rest. Exploratory analyses showed that MSL-related brain patterns in the posterior hippocampus persisted into post-learning rest preferentially after inhibitory stimulation. These results collectively show that prefrontal stimulation can alter multivoxel brain patterns in deep brain regions that are critical for the MSL process. They also suggest that stimulation influenced early offline consolidation processes as evidenced by a stimulation-induced modulation of the reinstatement of task pattern into post-learning wakeful rest. |
| first_indexed | 2024-12-21T05:01:23Z |
| format | Article |
| id | doaj.art-ea08bd8f3c64499999dca053e65a6161 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-21T05:01:23Z |
| publishDate | 2021-10-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-ea08bd8f3c64499999dca053e65a61612022-12-21T19:15:14ZengNature PortfolioScientific Reports2045-23222021-10-0111111410.1038/s41598-021-99926-1Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampusMareike A. Gann0Bradley R. King1Nina Dolfen2Menno P. Veldman3Marco Davare4Stephan P. Swinnen5Dante Mantini6Edwin M. Robertson7Geneviève Albouy8Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU LeuvenDepartment of Health and Kinesiology, College of Health, University of UtahDepartment of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU LeuvenDepartment of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU LeuvenDepartment of Clinical Sciences, College of Health and Life Sciences, Brunel University LondonDepartment of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU LeuvenDepartment of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU LeuvenInstitute of Neuroscience and Psychology, University of GlasgowDepartment of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU LeuvenAbstract Motor sequence learning (MSL) is supported by dynamical interactions between hippocampal and striatal networks that are thought to be orchestrated by the prefrontal cortex. In the present study, we tested whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex (DLPFC) prior to MSL can modulate multivoxel response patterns in the stimulated cortical area, the hippocampus and the striatum. Response patterns were assessed with multivoxel correlation structure analyses of functional magnetic resonance imaging data acquired during task practice and during resting-state scans before and after learning/stimulation. Results revealed that, across stimulation conditions, MSL induced greater modulation of task-related DLPFC multivoxel patterns than random practice. A similar learning-related modulatory effect was observed on sensorimotor putamen patterns under inhibitory stimulation. Furthermore, MSL as well as inhibitory stimulation affected (posterior) hippocampal multivoxel patterns at post-intervention rest. Exploratory analyses showed that MSL-related brain patterns in the posterior hippocampus persisted into post-learning rest preferentially after inhibitory stimulation. These results collectively show that prefrontal stimulation can alter multivoxel brain patterns in deep brain regions that are critical for the MSL process. They also suggest that stimulation influenced early offline consolidation processes as evidenced by a stimulation-induced modulation of the reinstatement of task pattern into post-learning wakeful rest.https://doi.org/10.1038/s41598-021-99926-1 |
| spellingShingle | Mareike A. Gann Bradley R. King Nina Dolfen Menno P. Veldman Marco Davare Stephan P. Swinnen Dante Mantini Edwin M. Robertson Geneviève Albouy Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus Scientific Reports |
| title | Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus |
| title_full | Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus |
| title_fullStr | Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus |
| title_full_unstemmed | Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus |
| title_short | Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus |
| title_sort | prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus |
| url | https://doi.org/10.1038/s41598-021-99926-1 |
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