Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulation
IntroductionTranscranial 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 loc...
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2023.1004763/full |
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| author | Brice Passera Brice Passera Brice Passera Sylvain Harquel Sylvain Harquel Sylvain Harquel Alan Chauvin Pauline Gérard Lisa Lai Elena Moro Sara Meoni Valerie Fraix Olivier David Olivier David Estelle Raffin Estelle Raffin |
| author_facet | Brice Passera Brice Passera Brice Passera Sylvain Harquel Sylvain Harquel Sylvain Harquel Alan Chauvin Pauline Gérard Lisa Lai Elena Moro Sara Meoni Valerie Fraix Olivier David Olivier David Estelle Raffin Estelle Raffin |
| author_sort | Brice Passera |
| collection | DOAJ |
| description | IntroductionTranscranial 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.MethodsSix 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.ResultsIn 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).ConclusionTaken 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. |
| first_indexed | 2024-04-09T14:26:37Z |
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| id | doaj.art-e82a1caaa434451bb17cd12c2a99754e |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-09T14:26:37Z |
| publishDate | 2023-05-01 |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-e82a1caaa434451bb17cd12c2a99754e2023-05-04T04:18:28ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-05-011710.3389/fnins.2023.10047631004763Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulationBrice Passera0Brice Passera1Brice Passera2Sylvain Harquel3Sylvain Harquel4Sylvain Harquel5Alan Chauvin6Pauline Gérard7Lisa Lai8Elena Moro9Sara Meoni10Valerie Fraix11Olivier David12Olivier David13Estelle Raffin14Estelle Raffin15CNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, FranceUniv. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, FranceBerenson-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 StatesCNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, FranceCNRS, INSERM, IRMaGe, Grenoble, FranceDefitech Chair in Clinical Neuroengineering, Neuro-X Institute and Brain Mind Institute, EPFL, Geneva, SwitzerlandCNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, FranceCNRS UMR 5105, Laboratoire Psychologie et Neurocognition, LPNC, Grenoble, FranceUniv. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, FranceUniv. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, FranceUniv. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, FranceUniv. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, FranceUniv. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, FranceAix Marseille Univ, Inserm, U1106, INS, Institut de Neurosciences des Systèmes, Marseille, FranceUniv. Grenoble Alpes, Inserm, U1216, CHU Grenoble Alpes, Grenoble Institut Neurosciences, Grenoble, FranceDefitech Chair in Clinical Neuroengineering, Neuro-X Institute and Brain Mind Institute, EPFL, Geneva, SwitzerlandIntroductionTranscranial 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.MethodsSix 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.ResultsIn 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).ConclusionTaken 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.https://www.frontiersin.org/articles/10.3389/fnins.2023.1004763/fullParkinson’s diseasedeep brain stimulationtranscranial magnetic stimulationTMS-EMG mappingTMS-EEG mappingstate-dependent mapping |
| spellingShingle | Brice Passera Brice Passera Brice Passera Sylvain Harquel Sylvain Harquel Sylvain Harquel Alan Chauvin Pauline Gérard Lisa Lai Elena Moro Sara Meoni Valerie Fraix Olivier David Olivier David Estelle Raffin Estelle Raffin Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulation Frontiers in Neuroscience Parkinson’s disease deep brain stimulation transcranial magnetic stimulation TMS-EMG mapping TMS-EEG mapping state-dependent mapping |
| title | Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulation |
| title_full | Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulation |
| title_fullStr | Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulation |
| title_full_unstemmed | Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulation |
| title_short | Multi-scale and cross-dimensional TMS mapping: A proof of principle in patients with Parkinson’s disease and deep brain stimulation |
| title_sort | multi scale and cross dimensional tms mapping a proof of principle in patients with parkinson s disease and deep brain stimulation |
| topic | Parkinson’s disease deep brain stimulation transcranial magnetic stimulation TMS-EMG mapping TMS-EEG mapping state-dependent mapping |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2023.1004763/full |
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