Motor adaptation and internal model formation in a robot-mediated forcefield

Article


Taga, M., Curci, A., Pizzamiglio, S., Lacal, I., Turner, D. and Fu, C. 2021. Motor adaptation and internal model formation in a robot-mediated forcefield. Psychoradiology. 1 (2), p. 73–87. https://doi.org/10.1093/psyrad/kkab007
AuthorsTaga, M., Curci, A., Pizzamiglio, S., Lacal, I., Turner, D. and Fu, C.
Abstract

Background: Motor adaptation relies on error-based learning for accurate movements in changing environments. However, the neurophysiological mechanisms driving individual differences in performance are unclear. TMS-evoked potential can provide a direct measure of cortical excitability.
Objective: To investigate cortical excitability as a predictor of motor learning and motor adaptation in a robot-mediated forcefield.
Methods: 15 right-handed healthy participants (mean age 23 years) performed a robot-mediated forcefield perturbation task. There were 2 conditions: unperturbed non-adaptation and perturbed adaptation. Transcranial magnetic stimulation (TMS) was applied in the resting state at baseline and following motor adaptation over the contralateral primary motor cortex (left M1). EEG was continuously recorded, and cortical excitability was measured by TMS-evoked potential (TEP). Motor learning was quantified by the motor learning index.
Results: Larger error-related negativity (ERN) in fronto-central regions was associated with improved motor performance as measured by a reduction in trajectory errors. Baseline TEP N100 peak amplitude predicted motor learning (p = 0.005), which was significantly attenuated relative to baseline (p = 0.0018) following motor adaptation.
Conclusions: ERN reflected the formation of a predictive internal model adapted to the forcefield perturbation. Attenuation in TEP N100 amplitude reflected an increase in cortical excitability with motor adaptation reflecting neuroplastic changes in the sensorimotor cortex. TEP N100 is a potential biomarker for predicting the outcome in robot-mediated therapy and a mechanism to investigate psychomotor abnormalities in depression.

JournalPsychoradiology
Journal citation1 (2), p. 73–87
ISSN2634-4416
Year2021
PublisherOxford University Press for West China School of Medicine/ West China Hospital (WCSM/WCH) of Sichuan University
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Digital Object Identifier (DOI)https://doi.org/10.1093/psyrad/kkab007
Publication dates
Online12 Jun 2021
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Accepted15 May 2021
Deposited13 May 2021
FunderMedical Research Council (MRC)
Copyright holder© 2021 The Authors
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Inkster, Becky, Simmons, Andy, Cole, James, Schoof, Erwin, Linding, Rune, Nichols, Tom, Muglia, Pierandrea, Holsboer, Florian, Saemann, Philipp, McGuffin, Peter, Fu, C., Miskowiak, Kamilla, Matthews, Paul M., Zai, Gwyneth and Nicodemus, Kristin 2018. Unravelling the GSK3β-related genotypic interaction network influencing hippocampal volume in recurrent major depressive disorder. Psychiatric Genetics. 28 (5), pp. 77-84. https://doi.org/10.1097/YPG.0000000000000203
Associations between polygenic risk scores for four psychiatric illnesses and brain structure using multivariate pattern recognition
Ranlund, Siri, Rosa, Maria Joao, de Jong, Simone, Cole, James H., Kyriakopoulos, Marinos, Fu, C., Mehta, Mitul A. and Dima, Danai 2018. Associations between polygenic risk scores for four psychiatric illnesses and brain structure using multivariate pattern recognition. NeuroImage: Clinical. 20, pp. 1026-1036. https://doi.org/10.1016/j.nicl.2018.10.008
Anodal transcranial direct current stimulation over the right dorsolateral prefrontal cortex enhances reflective judgment & decision-making
Edgcumbe, Daniel R., Thoma, V., Rivolta, Davide, Nitsche, Michael A. and Fu, C. 2018. Anodal transcranial direct current stimulation over the right dorsolateral prefrontal cortex enhances reflective judgment & decision-making. Brain Stimulation. 12 (3), pp. 652-658. https://doi.org/10.1016/j.brs.2018.12.003
Advanced technology for gait rehabilitation --- An overview
Mikolajczyk, Tadeusz, Ciobanu, Ileana, Badea, Joana, Iliescu, Alina, Pizzamiglio, S., Schauer, Thomas, See, Thomas, Seicu, Lucien, Turner, D. and Berteanu, Mihai 2018. Advanced technology for gait rehabilitation --- An overview. Advances in Mechanical Engineering. 10 (7), pp. 1-19. https://doi.org/10.1177/1687814018783627
Neural correlates of single- and dual-task walking in the real world
Pizzamiglio, Sara, Naeem, U., Abdalla, H. and Turner, D. 2017. Neural correlates of single- and dual-task walking in the real world. Frontiers in Human Neuroscience. 11, p. Art 460. https://doi.org/10.3389/fnhum.2017.00460
Effects of antidepressant therapy on neural components of verbal working memory in depression
Sankar, Anjali, Adams, Tracey M, Costafreda, Sergi G. and Fu, C. 2017. Effects of antidepressant therapy on neural components of verbal working memory in depression. Journal of Psychopharmacology. 31 (9), pp. 1176-1183. https://doi.org/10.1177/0269881117724594
Robot Assisted Training for the Upper Limb after Stroke (RATULS): study protocol for a randomised controlled trial
Rodgers, Helen, Shaw, Lisa, Bosomworth, Helen, Aird, Lydia, Alvarado, Natasha, Andole, Sreeman, Cohen, David L., Dawson, Jesse, Eyre, Janet, Finch, Tracy, Ford, Gary A., Hislop, Jennifer, Hogg, Steven, Howel, Denise, Hughes, Niall, Krebs, Hermano Igo, Price, Christopher, Rochester, Lynn, Stamp, Elaine, Ternent, Laura, Turner, D., Vale, Luke, Warburton, Elizabeth, van Wijck, Frederike and Wilkes, Scott 2017. Robot Assisted Training for the Upper Limb after Stroke (RATULS): study protocol for a randomised controlled trial. Trials. 18, p. Art. 340. https://doi.org/10.1186/s13063-017-2083-4
Body mass index, but not FTO genotype or major depressive disorder, influences brain structure
Cole, J.H., Boyle, C.P., Simmons, A., Cohen-Woods, S., Rivera, M., McGuffin, P., Thompson, P.M. and Fu, C. 2013. Body mass index, but not FTO genotype or major depressive disorder, influences brain structure. Neuroscience. 252 (Nov.), pp. 109-117. https://doi.org/10.1016/j.neuroscience.2013.07.015
Classification of Major Depressive Disorder via Multi-Site Weighted LASSO Model
Zhu, Dajiang, Riedel, Brandalyn C., Jahanshad, Neda, Groenewold, Nynke A., Stein, Dan J., Gotlib, Ian H., Dima, Danai, Cole, James H., Fu, C., Walter, Henrik, Veer, Ilya M., Frodl, Thomas, Schmaal, Lianne, Veltman, Dick J. and Thompson, Paul M. 2017. Classification of Major Depressive Disorder via Multi-Site Weighted LASSO Model. in: Descoteaux, Maxime, Maier-Hein, Lena, Franz, Alfred, Jannin, Pierre, Collins, D. Louis and Duchesne, Simon (ed.) Medical Image Computing and Computer-Assisted Intervention − MICCAI 2017 Springer, Cham.
Recent Advances in Neuroimaging of Mood Disorders: Structural and Functional Neural Correlates of Depression, Changes with Therapy, and Potential for Clinical Biomarkers
Atkinson, Lauren, Sankar, Anjali, Adams, Tracey M. and Fu, C. 2014. Recent Advances in Neuroimaging of Mood Disorders: Structural and Functional Neural Correlates of Depression, Changes with Therapy, and Potential for Clinical Biomarkers. Current Treatment Options in Psychiatry. 1 (3), pp. 278-293. https://doi.org/10.1007/s40501-014-0022-5
Common and distinct patterns of grey-matter volume alteration in major depression and bipolar disorder: evidence from voxel-based meta-analysis
Wise, T., Radua, J., Via, E., Cardoner, N., Abe, O., Adams, T. M., Amico, F., Cheng, Y., Cole, J. H., de Azevedo Marques Périco, C., Dickstein, D. P., Farrow, T. F. D., Frodl, T., Wagner, G., Gotlib, I. H., Gruber, O., Ham, B. J., Job, D. E., Kempton, M. J., Kim, M. J., Koolschijn, P. C. M. P., Malhi, G. S., Mataix-Cols, D., McIntosh, A. M., Nugent, A. C., O'Brien, J. T.., Pezzoli, S, Phillips, M. L., Sachdev, P. S., Salvadore, G., Selvaraj, S., Stanfield, A. C., Thomas, A. J., van Tol, M. J., van der Wee, N. J. A., Veltman, D. J., Young, A. H., Fu, C., Cleare, A. J. and Arnone, D. 2016. Common and distinct patterns of grey-matter volume alteration in major depression and bipolar disorder: evidence from voxel-based meta-analysis. Molecular Psychiatry. https://doi.org/10.1038/mp.2016.72
High-Frequency Intermuscular Coherence between Arm Muscles during Robot-Mediated Motor Adaptation
Pizzamiglio, Sara, De Lillo, Martina, Naeem, U., Abdalla, Hassan and Turner, D. 2017. High-Frequency Intermuscular Coherence between Arm Muscles during Robot-Mediated Motor Adaptation. Frontiers in Physiology. 7 (668), pp. 1-14. https://doi.org/10.3389/fphys.2016.00668
Muscle co-contraction patterns in robot-mediated force field learningto guide specific muscle group training
Pizzamiglio, S., Desowska, A., Mohajer Shojaii, P., Taga, M. and Turner, D. 2017. Muscle co-contraction patterns in robot-mediated force field learningto guide specific muscle group training. NeuroRehabilitation. 41 (1), pp. 17-29. https://doi.org/10.3233/NRE-171453
A Mutlimodal Approach to Measure the Levels Distraction of Pedestrians using Mobile Sensing
Pizzamiglio, S., Naeem, U., ur Réhman, Shafiq, Sharif, M., Abdalla, H. and Turner, D. 2017. A Mutlimodal Approach to Measure the Levels Distraction of Pedestrians using Mobile Sensing. Procedia Computer Science. 113, pp. 89-96. https://doi.org/10.1016/j.procs.2017.08.297
Diagnostic potential of structural neuroimaging for depression from a multi-ethnic community sample
Sankar, Anjali, Zhang, Tianhao, Gaonkar, Bilwaj, Doshi, Jimit, Erus, Guray, Costafreda, Sergi G., Marangell, Lauren, Davatzikos, Christos and Fu, C. 2016. Diagnostic potential of structural neuroimaging for depression from a multi-ethnic community sample. BJPsych Open. 2 (4), pp. 247-254. https://doi.org/10.1192/bjpo.bp.115.002493
Real-time functional magnetic resonance imaging neurofeedback in motor neurorehabilitation
Linden, David E.J. and Turner, D. 2016. Real-time functional magnetic resonance imaging neurofeedback in motor neurorehabilitation. Current Opinion in Neurology. 29 (4), pp. 412-418. https://doi.org/10.1097/WCO.0000000000000340
Functional Magnetic Resonance Imaging Neurofeedback-guided Motor Imagery Training and Motor Training for Parkinson’s Disease: Randomized Trial
Subramanian, Leena, Busse-Morris, Monica, Brosnan, Meadhbh, Turner, D., Morris, Huw R. and Linden, David E. J. 2016. Functional Magnetic Resonance Imaging Neurofeedback-guided Motor Imagery Training and Motor Training for Parkinson’s Disease: Randomized Trial. Frontiers in Behavioural Neuroscience. 10, p. Art.111. https://doi.org/10.3389/fnbeh.2016.00111
Meta-analyses of structural regional cerebral effects in type 1 and type 2 diabetes
Moulton, Calum D., Costafreda, Sergi G., Horton, Paul, Ismail, Khalida and Fu, C. 2015. Meta-analyses of structural regional cerebral effects in type 1 and type 2 diabetes. Brain Imaging and Behavior. 9 (4), pp. 651-662.
A systematic review of the neurophysiology of mindfulness on EEG oscillations
Lomas, T., Ivtzan, I. and Fu, C. 2015. A systematic review of the neurophysiology of mindfulness on EEG oscillations. Neuroscience & Biobehavioral Reviews. 57, pp. 401-410.
Spinal plasticity in robot-mediated therapy for the lower limbs
Stevenson, Andrew JT, Mrachacz-Kersting, Natalie, van Asseldonk, Edwin, Turner, D. and Spaich, Erika G. 2015. Spinal plasticity in robot-mediated therapy for the lower limbs. Journal of NeuroEngineering and Rehabilitation. 12 (1).
Multimodal functional and structural neuroimaging investigation of major depressive disorder following treatment with duloxetine
Fu, C., Costafreda, Sergi G, Sankar, Anjali, Adams, Tracey M, Rasenick, Mark M, Liu, Peng, Donati, Robert, Maglanoc, Luigi A, Horton, Paul and Marangell, Lauren B 2015. Multimodal functional and structural neuroimaging investigation of major depressive disorder following treatment with duloxetine. BMC Psychiatry. 15 (1).
Neural effects of cognitive–behavioural therapy on dysfunctional attitudes in depression
Sankar, A., Scott, J., Paszkiewicz, A., Giampietro, V. P., Steiner, H. and Fu, C. 2014. Neural effects of cognitive–behavioural therapy on dysfunctional attitudes in depression. Psychological Medicine. 45 (7), pp. 1425-1433.
Neurophysiology of Robot-Mediated Training and Therapy: A Perspective for Future Use in Clinical Populations
Turner, D., Ramos-Murguialday, Ander, Birbaumer, Niels, Hoffmann, Ulrich and Luft, Andreas 2013. Neurophysiology of Robot-Mediated Training and Therapy: A Perspective for Future Use in Clinical Populations. Frontiers in Neurology. 4 (184).
Modulatory effects of brain-derived neurotrophic factor Val66Met polymorphism on prefrontal regions in major depressive disorder
Legge, R. M., Sendi, S., Cole, J. H., Cohen-Woods, S., Costafreda, S. G., Simmons, A., Farmer, A. E., Aitchison, K. J., McGuffin, P. and Fu, C. 2015. Modulatory effects of brain-derived neurotrophic factor Val66Met polymorphism on prefrontal regions in major depressive disorder. The British Journal of Psychiatry. 206 (5), pp. 379-384.
Prognostic and Diagnostic Potential of the Structural Neuroanatomy of Depression
Domschke, Katharina, Costafreda, Sergi G., Chu, Carlton, Ashburner, John and Fu, C. 2009. Prognostic and Diagnostic Potential of the Structural Neuroanatomy of Depression. PLOS ONE. 4 (7), p. e6353.
Pattern of neural responses to verbal fluency shows diagnostic specificity for schizophrenia and bipolar disorder
Costafreda, Sergi G, Fu, C., Picchioni, Marco, Toulopoulou, Timothea, McDonald, Colm, Kravariti, Eugenia, Walshe, Muriel, Prata, Diana, Murray, Robin M and McGuire, Philip K 2011. Pattern of neural responses to verbal fluency shows diagnostic specificity for schizophrenia and bipolar disorder. BMC Psychiatry. 11 (1), p. 18.
Neuroimaging-Based Biomarkers in Psychiatry: Clinical Opportunities of a Paradigm Shift
Fu, C. and Costafreda, Sergi G. 2013. Neuroimaging-Based Biomarkers in Psychiatry: Clinical Opportunities of a Paradigm Shift. Canadian Journal of Psychiatry. 58 (9), pp. 499-508.
Neurophysiology of Robot-Mediated Training and Therapy: A Perspective for Future Use in Clinical Populations
Turner, D., Ramos-Murguialday, Ander, Birbaumer, Niels, Hoffmann, Ulrich and Luft, Andreas 2013. Neurophysiology of Robot-Mediated Training and Therapy: A Perspective for Future Use in Clinical Populations. Frontiers in Neurology. 4 (184).
Modulation of internal model formation during force field-induced motor learning by anodal transcranial direct current stimulation of primary motor cortex
Hunter, Timothy, Sacco, Paul, Nitsche, Michael A. and Turner, D. 2009. Modulation of internal model formation during force field-induced motor learning by anodal transcranial direct current stimulation of primary motor cortex. Journal of Physiology. 587 (12).