DBS-TMS paired-pulse mapping; Parkinson’s disease; TMS-EEG mapping; TMS-EMG mapping; deep brain stimulation; state-dependent mapping; transcranial magnetic stimulation; Neuroscience (all)
Abstract :
[en] [en] INTRODUCTION: Transcranial magnetic stimulation (TMS) mapping has become a critical tool for exploratory studies of the human corticomotor (M1) organization. Here, we propose to gather existing cutting-edge TMS-EMG and TMS-EEG approaches into a combined multi-dimensional TMS mapping that considers local and whole-brain excitability changes as well as state and time-specific changes in cortical activity. We applied this multi-dimensional TMS mapping approach to patients with Parkinson's disease (PD) with Deep brain stimulation (DBS) of the sub-thalamic nucleus (STN) ON and OFF. Our goal was to identifying one or several TMS mapping-derived markers that could provide unprecedent new insights onto the mechanisms of DBS in movement disorders.
METHODS: Six PD patients (1 female, mean age: 62.5 yo [59-65]) implanted with DBS-STN for 1 year, underwent a robotized sulcus-shaped TMS motor mapping to measure changes in muscle-specific corticomotor representations and a movement initiation task to probe state-dependent modulations of corticospinal excitability in the ON (using clinically relevant DBS parameters) and OFF DBS states. Cortical excitability and evoked dynamics of three cortical areas involved in the neural control of voluntary movements (M1, pre-supplementary motor area - preSMA and inferior frontal gyrus - IFG) were then mapped using TMS-EEG coupling in the ON and OFF state. Lastly, we investigated the timing and nature of the STN-to-M1 inputs using a paired pulse DBS-TMS-EEG protocol.
RESULTS: In our sample of patients, DBS appeared to induce fast within-area somatotopic re-arrangements of motor finger representations in M1, as revealed by mediolateral shifts of corticomuscle representations. STN-DBS improved reaction times while up-regulating corticospinal excitability, especially during endogenous motor preparation. Evoked dynamics revealed marked increases in inhibitory circuits in the IFG and M1 with DBS ON. Finally, inhibitory conditioning effects of STN single pulses on corticomotor activity were found at timings relevant for the activation of inhibitory GABAergic receptors (4 and 20 ms).
CONCLUSION: Taken together, these results suggest a predominant role of some markers in explaining beneficial DBS effects, such as a context-dependent modulation of corticospinal excitability and the recruitment of distinct inhibitory circuits, involving long-range projections from higher level motor centers and local GABAergic neuronal populations. These combined measures might help to identify discriminative features of DBS mechanisms towards deep clinical phenotyping of DBS effects in Parkinson's Disease and in other pathological conditions.
Disciplines :
Neurosciences & behavior
Author, co-author :
Passera, Brice; CNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, France ; Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, France ; Berenson-Allen Center for Noninvasive Brain Stimulation, Division of Cognitive Neurology, Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, MA, United States
Harquel, Sylvain; CNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, France ; CNRS, INSERM, IRMaGe, Grenoble, France ; Defitech Chair in Clinical Neuroengineering, Neuro-X Institute and Brain Mind Institute, EPFL, Geneva, Switzerland
Chauvin, Alan; CNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, France
Gérard, Pauline; CNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, France
LAI, Lisa ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS) > Health and Behaviour ; Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, France
David, Olivier; Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, France ; Aix Marseille Univ, Inserm, U1106, INS, Institut de Neurosciences des Systèmes, Marseille, France
Raffin, Estelle; Univ. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, France ; Defitech Chair in Clinical Neuroengineering, Neuro-X Institute and Brain Mind Institute, EPFL, Geneva, Switzerland
External co-authors :
yes
Language :
English
Title :
Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson's disease and deep brain stimulation.
This work was funded by the Agence Nationale pour la Recherche grant “ANR-15-CE37-0015-1” and by NeuroCoG IDEX UGA in the framework of the “Investissements d’avenir” program (ANR-15-IDEX-02). Data were acquired on a platform of France Life Imaging Network partly funded by the grant “ANR-11-INBS-0006.”
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