Prefrontal stimulation as a tool to disrupt hippocampal and striatal reactivations underlying fast motor memory consolidation

Gann, M. A., Dolfen, N., King, B. R., Robertson, E. M. and Albouy, G. (2023) Prefrontal stimulation as a tool to disrupt hippocampal and striatal reactivations underlying fast motor memory consolidation. Brain Stimulation, 16(5), pp. 1336-1345. (doi: 10.1016/j.brs.2023.08.022) (PMID:37647985)

Abstract

Background Recent evidence suggests that hippocampal replay in humans support rapid motor memory consolidation during epochs of wakefulness interleaved with task practice. Objectives/Hypotheses The goal of this study was to test whether such reactivation patterns can be modulated with experimental interventions and in turn influence fast consolidation. We hypothesized that non-invasive brain stimulation targeting hippocampal and striatal networks via the prefrontal cortex would influence brain reactivation and the rapid form of motor memory consolidation. Methods Theta-burst stimulation was applied to a prefrontal cluster functionally connected to both the hippocampus and striatum of young healthy participants before they learned a motor sequence task in a functional magnetic resonance imaging (fMRI) scanner. Neuroimaging data acquired during task practice and the interleaved rest epochs were analyzed to comprehensively characterize the effect of stimulation on the neural processes supporting fast motor memory consolidation. Results Our results collectively show that active, as compared to control, theta-burst stimulation of the prefrontal cortex hindered fast motor memory consolidation. Converging evidence from both univariate and multivariate analyses of fMRI data indicate that active stimulation disrupted hippocampal and caudate responses during inter-practice rest, presumably altering the reactivation of learning-related patterns during the micro-offline consolidation episodes. Last, stimulation altered the link between the brain and the behavioral markers of the fast consolidation process. Conclusion These results suggest that stimulation targeting deep brain regions via the prefrontal cortex can be used to modulate hippocampal and striatal reactivations in the human brain and influence motor memory consolidation.

• Item Type: Articles
• Additional Information: This 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). MAG and ND 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 Office of Scientific Research (AFOSR, Virginia, USA; FA9550-16-1-0191).
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Robertson, Professor Edwin

Creator Roles

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

• Authors: Gann, M. A., Dolfen, N., King, B. R., Robertson, E. M., and Albouy, G.
• College/School: College of Medical Veterinary and Life Sciences > School of Psychology & Neuroscience
• Journal Name: Brain Stimulation
• Publisher: Elsevier
• ISSN: 1935-861X
• ISSN (Online): 1876-4754
• Published Online: 11 September 2023
• Copyright Holders: Copyright: © 2023 The Authors
• First Published: First published in Brain Stimulation 16(5): 1336-1345
• Publisher Policy: Reproduced under a Creative Commons licence
• Data DOI: 10.5281/zenodo.8233881