Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus

Gann, M. A., King, B. R., Dolfen, N., Veldman, M. P., Davare, M., Swinnen, S. P., Mantini, D., Robertson, E. M. and Albouy, G. (2021) Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus. Scientific Reports, 11, 20572. (doi: 10.1038/s41598-021-99926-1) (PMID:34663890) (PMCID:PMC8523553)

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.

• Item Type: Articles
• Additional Information: Tis work was supported by the Belgian Research Foundation Flanders (FWO; G099516N) and internal funds from KU Leuven. GA also received support from FWO (G0D7918N, G0B1419N, 1524218N) and Excellence of Science (EOS, 30446199, MEMODYN, with SPS and DM). MAG, ND and MPV received salary support from these grants. MAG is funded by a predoctoral fellowship from FWO (1141320N). Financial support for author BRK was provided by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement (703490) and a postdoctoral fellowship from FWO (132635). EMR received salary support from the Air Force Ofce of Scientifc Research (AFOSR, Virginia, USA; FA9550-16-1-0191).
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Robertson, Professor Edwin

Creator Roles

Robertson, E. M.: Conceptualization, Writing – review and editing

• Authors: Gann, M. A., King, B. R., Dolfen, N., Veldman, M. P., Davare, M., Swinnen, S. P., Mantini, D., Robertson, E. M., and Albouy, G.
• College/School: College of Medical Veterinary and Life Sciences > School of Psychology & Neuroscience
• Journal Name: Scientific Reports
• Publisher: Nature Research
• ISSN: 2045-2322
• ISSN (Online): 2045-2322
• Copyright Holders: Copyright © The Author(s) 2021
• First Published: First published in Scientific Reports 11:20572
• Publisher Policy: Reproduced under a Creative Commons Licence