Hippocampal and striatal responses during motor learning are modulated by prefrontal cortex stimulation
Mareike A. Gann,
Bradley R. King,
Nina Dolfen,
Menno P. Veldman,
Kimberly L. Chan,
Nicolaas A.J. Puts,
Richard A.E. Edden,
Marco Davare,
Stephan P. Swinnen,
Dante Mantini,
Edwin M. Robertson,
Geneviève Albouy
Affiliations
Mareike A. Gann
Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU Leuven, 3001 Leuven, Belgium; LBI - KU Leuven Brain Institute, KU Leuven, 3001 Leuven, Belgium
Bradley R. King
Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU Leuven, 3001 Leuven, Belgium; LBI - KU Leuven Brain Institute, KU Leuven, 3001 Leuven, Belgium
Nina Dolfen
Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU Leuven, 3001 Leuven, Belgium; LBI - KU Leuven Brain Institute, KU Leuven, 3001 Leuven, Belgium
Menno P. Veldman
Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU Leuven, 3001 Leuven, Belgium; LBI - KU Leuven Brain Institute, KU Leuven, 3001 Leuven, Belgium
Kimberly L. Chan
Advanced Imaging Research Center, University of Texas Southwestern, Dallas, TX 75390, USA
Nicolaas A.J. Puts
The Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; F. M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD 21205, USA; Department of Forensic and Neurodevelopmental Sciences and the Institute of Psychiatry, Psychology, and Neuroscience; King's College London, SE5 8AF London, United Kingdom
Richard A.E. Edden
The Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; F. M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD 21205, USA
Marco Davare
Department of Clinical Sciences, College of Health and Life Sciences, Brunel University London, UB8 3PN Uxbridge, United Kingdom
Stephan P. Swinnen
Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU Leuven, 3001 Leuven, Belgium; LBI - KU Leuven Brain Institute, KU Leuven, 3001 Leuven, Belgium
Dante Mantini
Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU Leuven, 3001 Leuven, Belgium; Brain Imaging and Neural Dynamics Research Group, IRCCS San Camillo Hospital, 30126 Venice, Italy
Edwin M. Robertson
Institute of Neuroscience and Psychology, University of Glasgow, G12 8QB Glasgow, United Kingdom
Geneviève Albouy
Department of Movement Sciences, Movement Control and Neuroplasticity Research Group, KU Leuven, 3001 Leuven, Belgium; LBI - KU Leuven Brain Institute, KU Leuven, 3001 Leuven, Belgium; Corresponding author at: Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, KU Leuven, Tervuursevest 101 - Box 1501, 3001 Leuven, Belgium.
While it is widely accepted that motor sequence learning (MSL) is supported by a prefrontal-mediated interaction between hippocampal and striatal networks, it remains unknown whether the functional responses of these networks can be modulated in humans with targeted experimental interventions. The present proof-of-concept study employed a multimodal neuroimaging approach, including functional magnetic resonance (MR) imaging and MR spectroscopy, to investigate whether individually-tailored theta-burst stimulation of the dorsolateral prefrontal cortex can modulate responses in the hippocampus and the basal ganglia during motor learning. Our results indicate that while stimulation did not modulate motor performance nor task-related brain activity, it influenced connectivity patterns within hippocampo-frontal and striatal networks. Stimulation also altered the relationship between the levels of gamma-aminobutyric acid (GABA) in the stimulated prefrontal cortex and learning-related changes in both activity and connectivity in fronto-striato-hippocampal networks. This study provides the first experimental evidence, to the best of our knowledge, that brain stimulation can alter motor learning-related functional responses in the striatum and hippocampus.
