Neural Signatures of Motor Skill in the Resting Brain

Stroke-induced disturbances of large-scale cortical networks are known to be associated with the extent of motor deficits. We argue that identifying brain networks representative of motor behavior in the resting brain would provide significant insights for current neurorehabilitation approaches. Particularly, we aim to investigate the global configuration of brain rhythms and their relation to motor skill, instead of learning performance as broadly studied. We empirically approach this problem by conducting a three-dimensional physical space visuomotor learning experiment during electroencephalographic (EEG) data recordings with thirty-seven healthy participants. We demonstrate that across-subjects variations in average movement smoothness as the quantified measure of subjects’ motor skills can be predicted from the global configuration of resting-state EEG alpha-rhythms (8–14 Hz) recorded prior to the experiment. Importantly, this neural signature of motor skill was found to be orthogonal to (independent of) task-as well as to learning-related changes in alpha-rhythms, which we interpret as an organizing principle of the brain. We argue that disturbances of such configurations in the brain may contribute to motor deficits in stroke, and that reconfiguring stroke patients’ brain rhythms by neurofeedback may enhance post-stroke neurorehabilitation.

[1]  A. Fugl-Meyer,et al.  The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. , 1975, Scandinavian journal of rehabilitation medicine.

[2]  Allen and Rosenbloom Paul S. Newell,et al.  Mechanisms of Skill Acquisition and the Law of Practice , 1993 .

[3]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Peter J. Rousseeuw,et al.  Robust Regression and Outlier Detection , 2005, Wiley Series in Probability and Statistics.

[5]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[6]  Eric Moulines,et al.  A blind source separation technique using second-order statistics , 1997, IEEE Trans. Signal Process..

[7]  M. Hallett,et al.  Integrative visuomotor behavior is associated with interregionally coherent oscillations in the human brain. , 1998, Journal of neurophysiology.

[8]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[9]  N. Hogan,et al.  Quantization of continuous arm movements in humans with brain injury. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[10]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[11]  Robert Oostenveld,et al.  The five percent electrode system for high-resolution EEG and ERP measurements , 2001, Clinical Neurophysiology.

[12]  Kae Nakamura,et al.  Central mechanisms of motor skill learning , 2002, Current Opinion in Neurobiology.

[13]  N. Hogan,et al.  Movement Smoothness Changes during Stroke Recovery , 2002, The Journal of Neuroscience.

[14]  William S. Harwin,et al.  Minimum Jerk Trajectory Control for Rehabilitation and Haptic Applications , 2002, ICRA.

[15]  B. Bhakta,et al.  Measuring movement irregularity in the upper motor neurone syndrome using normalised average rectified jerk. , 2003, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[16]  D. Tucker,et al.  Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation , 2004, Clinical Neurophysiology.

[17]  N. Birbaumer,et al.  BCI2000: a general-purpose brain-computer interface (BCI) system , 2004, IEEE Transactions on Biomedical Engineering.

[18]  Steven C Cramer,et al.  Robotics, motor learning, and neurologic recovery. , 2004, Annual review of biomedical engineering.

[19]  Hirokazu Seki,et al.  Minimum jerk control of power assisting robot on human arm behavior characteristic , 2004, 2004 IEEE International Conference on Systems, Man and Cybernetics (IEEE Cat. No.04CH37583).

[20]  J. Krakauer Motor learning: its relevance to stroke recovery and neurorehabilitation. , 2006, Current opinion in neurology.

[21]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[22]  R. Shadmehr,et al.  Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor Learning , 2006, PLoS biology.

[23]  R. Barry,et al.  EEG differences between eyes-closed and eyes-open resting conditions , 2007, Clinical Neurophysiology.

[24]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[25]  L. Cohen,et al.  Brain–computer interfaces: communication and restoration of movement in paralysis , 2007, The Journal of physiology.

[26]  Scott T. Grafton,et al.  Evidence for a distributed hierarchy of action representation in the brain. , 2007, Human movement science.

[27]  J. Baron,et al.  Motor imagery after stroke: Relating outcome to motor network connectivity , 2009, Annals of neurology.

[28]  S. Bressler,et al.  Large-scale brain networks in cognition: emerging methods and principles , 2010, Trends in Cognitive Sciences.

[29]  J. Peters,et al.  Closing the sensorimotor loop: haptic feedback facilitates decoding of motor imagery , 2011, Journal of neural engineering.

[30]  A. Rilk,et al.  Alpha coherence predicts accuracy during a visuomotor tracking task , 2011, Neuropsychologia.

[31]  Scott T. Grafton,et al.  Dynamic reconfiguration of human brain networks during learning , 2010, Proceedings of the National Academy of Sciences.

[32]  Moritz Grosse-Wentrup,et al.  Using brain–computer interfaces to induce neural plasticity and restore function , 2011, Journal of neural engineering.

[33]  J. Krakauer,et al.  Human sensorimotor learning: adaptation, skill, and beyond , 2011, Current Opinion in Neurobiology.

[34]  T. Milner,et al.  Functionally Specific Changes in Resting-State Sensorimotor Networks after Motor Learning , 2011, The Journal of Neuroscience.

[35]  R. Oostenveld,et al.  Independent EEG Sources Are Dipolar , 2012, PloS one.

[36]  Giuseppe Pagnoni,et al.  Altered resting-state effective connectivity of fronto-parietal motor control systems on the primary motor network following stroke , 2012, NeuroImage.

[37]  I. Howard,et al.  Perceiving in Depth, Volume 2 , 2012 .

[38]  V. Caggiano,et al.  Proprioceptive Feedback and Brain Computer Interface (BCI) Based Neuroprostheses , 2012, PloS one.

[39]  Laurence Dricot,et al.  Brain activations underlying different patterns of performance improvement during early motor skill learning , 2012, NeuroImage.

[40]  Müjdat Çetin,et al.  Brain Computer Interface based robotic rehabilitation with online modification of task speed , 2013, 2013 IEEE 13th International Conference on Rehabilitation Robotics (ICORR).

[41]  L. Cohen,et al.  Brain–machine interface in chronic stroke rehabilitation: A controlled study , 2013, Annals of neurology.

[42]  Jan Peters,et al.  Predicting motor learning performance from Electroencephalographic data , 2014, Journal of NeuroEngineering and Rehabilitation.

[43]  H. B. Meziane,et al.  Neural Activations during Visual Sequence Learning Leave a Trace in Post-Training Spontaneous EEG , 2013, PloS one.

[44]  M. Çetin,et al.  Towards Neurofeedback Training of Associative Brain Areas for Stroke Rehabilitation , 2014 .

[45]  Chunshui Yu,et al.  Altered Functional Organization within and between Resting-State Networks in Chronic Subcortical Infarction , 2014, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[46]  Cuntai Guan,et al.  Brain-computer interface-based robotic end effector system for wrist and hand rehabilitation: results of a three-armed randomized controlled trial for chronic stroke , 2014, Front. Neuroeng..

[47]  Sebastian Haufe,et al.  The role of alpha-rhythm states in perceptual learning: insights from experiments and computational models , 2014, Front. Comput. Neurosci..

[48]  Steven C. Cramer,et al.  Resting-state cortical connectivity predicts motor skill acquisition , 2014, NeuroImage.

[49]  T. Flash,et al.  The activity in the contralateral primary motor cortex, dorsal premotor and supplementary motor area is modulated by performance gains , 2014, Front. Hum. Neurosci..

[50]  M. Molinari,et al.  Brain–computer interface boosts motor imagery practice during stroke recovery , 2015, Annals of neurology.

[51]  Cuntai Guan,et al.  A Randomized Controlled Trial of EEG-Based Motor Imagery Brain-Computer Interface Robotic Rehabilitation for Stroke , 2015, Clinical EEG and neuroscience.

[52]  AlexanderThiel,et al.  Structural and Resting-State Brain Connectivity of Motor Networks After Stroke , 2015 .

[53]  M. Çetin,et al.  Electroencephalographic identifiers of motor adaptation learning , 2017, Journal of neural engineering.

[54]  Bernhard Schölkopf,et al.  Personalized brain-computer interface models for motor rehabilitation , 2017, 2017 IEEE International Conference on Systems, Man, and Cybernetics (SMC).

[55]  Moritz Grosse-Wentrup,et al.  Correlations of motor Adaptation Learning and modulation of resting-State sensorimotor EEG Activity , 2017, GBCIC.

[56]  Armin Schnider,et al.  Resting-state connectivity predicts visuo-motor skill learning , 2018, NeuroImage.