Different oscillatory entrainment of cortical networks during motor imagery and neurofeedback in right and left handers

Volitional modulation and neurofeedback of sensorimotor oscillatory activity is currently being evaluated as a strategy to facilitate motor restoration following stroke. Knowledge on the interplay between this regional brain self-regulation, distributed network entrainment and handedness is, however, limited. In a randomized cross-over design, twenty-one healthy subjects (twelve right-handers [RH], nine left-handers [LH]) performed kinesthetic motor imagery of left (48 trials) and right finger extension (48 trials). A brain-machine interface turned event-related desynchronization in the beta frequency-band (16-22 Hz) during motor imagery into passive hand opening by a robotic orthosis. Thereby, every participant subsequently activated either the dominant (DH) or non-dominant hemisphere (NDH) to control contralateral hand opening. The task-related cortical networks were studied with electroencephalography. The magnitude of the induced oscillatory modulation range in the sensorimotor cortex was independent of both handedness (RH, LH) and hemispheric specialization (DH, NDH). However, the regional beta-band modulation was associated with different alpha-band networks in RH and LH: RH presented a stronger inter-hemispheric connectivity, while LH revealed a stronger intra-hemispheric interaction. Notably, these distinct network entrainments were independent of hemispheric specialization. In healthy subjects, sensorimotor beta-band activity can be robustly modulated by motor imagery and proprioceptive feedback in both hemispheres independent of handedness. However, right and left handers show different oscillatory entrainment of cortical alpha-band networks during neurofeedback. This finding may inform neurofeedback interventions in future to align them more precisely with the underlying physiology.

[1]  O. Blanke,et al.  Differential influence of hands posture on mental rotation of hands and feet in left and right handers , 2009, Experimental Brain Research.

[2]  Alireza Gharabaghi,et al.  Oscillatory entrainment of the motor cortical network during motor imagery is modulated by the feedback modality , 2015, NeuroImage.

[3]  Saeid Sanei,et al.  EEG signal processing , 2000, Clinical Neurophysiology.

[4]  Mingzhou Ding,et al.  Attentional Modulation of Alpha Oscillations in Macaque Inferotemporal Cortex , 2011, The Journal of Neuroscience.

[5]  M. Corbetta,et al.  Frontoparietal Cortex Controls Spatial Attention through Modulation of Anticipatory Alpha Rhythms , 2009, The Journal of Neuroscience.

[6]  Alireza Gharabaghi,et al.  Estimating cognitive load during self-regulation of brain activity and neurofeedback with therapeutic brain-computer interfaces , 2015, Front. Behav. Neurosci..

[7]  Alireza Gharabaghi,et al.  Bridging the gap between motor imagery and motor execution with a brain–robot interface , 2015, NeuroImage.

[8]  A. Gharabaghi,et al.  Closed-loop adaptation of neurofeedback based on mental effort facilitates reinforcement learning of brain self-regulation , 2016, Clinical Neurophysiology.

[9]  Nick S. Ward,et al.  Beta oscillations reflect changes in motor cortex inhibition in healthy ageing , 2014, NeuroImage.

[10]  C. Braun,et al.  Prestimulus oscillatory power and connectivity patterns predispose conscious somatosensory perception , 2014, Proceedings of the National Academy of Sciences.

[11]  Anina N. Rich,et al.  Multimodal functional imaging of motor imagery using a novel paradigm , 2013, NeuroImage.

[12]  Alireza Gharabaghi,et al.  What is the optimal task difficulty for reinforcement learning of brain self-regulation? , 2016, Clinical Neurophysiology.

[13]  Alireza Gharabaghi,et al.  Recruitment of Additional Corticospinal Pathways in the Human Brain with State-Dependent Paired Associative Stimulation , 2018, The Journal of Neuroscience.

[14]  Giancarlo Ferrigno,et al.  Re-thinking the role of motor cortex: Context-sensitive motor outputs? , 2014, NeuroImage.

[15]  R. Romo,et al.  α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking , 2011, Proceedings of the National Academy of Sciences.

[16]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[17]  Martin V. Sale,et al.  Asymmetry of motor cortex excitability during a simple motor task: relationships with handedness and manual performance , 2001, Experimental Brain Research.

[18]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[19]  F. Babiloni,et al.  Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function , 2005, NeuroImage.

[20]  G. Pfurtscheller,et al.  Imagery of motor actions: differential effects of kinesthetic and visual-motor mode of imagery in single-trial EEG. , 2005, Brain research. Cognitive brain research.

[21]  C. Civardi,et al.  Hemispheric asymmetries of cortico-cortical connections in human hand motor areas , 2000, Clinical Neurophysiology.

[22]  U. Halsband,et al.  Motor learning in man: A review of functional and clinical studies , 2006, Journal of Physiology-Paris.

[23]  K. Müller,et al.  Robustly estimating the flow direction of information in complex physical systems. , 2007, Physical review letters.

[24]  Simone Rossi,et al.  Cortico-Cortical Connectivity between Right Parietal and Bilateral Primary Motor Cortices during Imagined and Observed Actions: A Combined TMS/tDCS Study , 2011, Front. Neural Circuits.

[25]  Alireza Gharabaghi,et al.  Predicting workload profiles of brain–robot interface and electromygraphic neurofeedback with cortical resting-state networks: personal trait or task-specific challenge? , 2015, Journal of neural engineering.

[26]  J. Palva,et al.  Functional Roles of Alpha-Band Phase Synchronization in Local and Large-Scale Cortical Networks , 2011, Front. Psychology.

[27]  Alireza Gharabaghi,et al.  Neuromuscular Plasticity: Disentangling Stable and Variable Motor Maps in the Human Sensorimotor Cortex , 2016, Neural plasticity.

[28]  Stephan F Taylor,et al.  Handedness, dexterity, and motor cortical representations. , 2011, Journal of neurophysiology.

[29]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[30]  Tony W. Wilson,et al.  Cue-related Temporal Factors Modulate Movement-related Beta Oscillatory Activity in the Human Motor Circuit , 2016, Journal of Cognitive Neuroscience.

[31]  V. Romei,et al.  Information-Based Approaches of Noninvasive Transcranial Brain Stimulation , 2016, Trends in Neurosciences.

[32]  L. McEvoy,et al.  Neurophysiological indices of strategy development and skill acquisition. , 1999, Brain research. Cognitive brain research.

[33]  Janice J. Eng,et al.  Individuals with the Dominant Hand Affected following Stroke Demonstrate Less Impairment Than Those with the Nondominant Hand Affected , 2006, Neurorehabilitation and neural repair.

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

[35]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[36]  Roel M. Willems,et al.  On the other hand: including left-handers in cognitive neuroscience and neurogenetics , 2014, Nature Reviews Neuroscience.

[37]  Alireza Gharabaghi,et al.  Brain State-Dependent Transcranial Magnetic Closed-Loop Stimulation Controlled by Sensorimotor Desynchronization Induces Robust Increase of Corticospinal Excitability , 2016, Brain Stimulation.

[38]  D. Wolpert,et al.  Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation , 2002, The Journal of physiology.

[39]  Mark Hallett,et al.  Timing-dependent modulation of the posterior parietal cortex-primary motor cortex pathway by sensorimotor training. , 2012, Journal of neurophysiology.

[40]  Jessica Cantillo-Negrete,et al.  An approach to improve the performance of subject-independent BCIs-based on motor imagery allocating subjects by gender , 2014, BioMedical Engineering OnLine.

[41]  J. Adair,et al.  Arm Use After Left or Right Hemiparesis Is Influenced by Hand Preference , 2009, Stroke.

[42]  S. Aglioti,et al.  The influence of hands posture on mental rotation of hands and feet , 2007, Experimental Brain Research.

[43]  Christa Neuper,et al.  Cue-induced beta rebound during withholding of overt and covert foot movement , 2012, Clinical Neurophysiology.

[44]  B. Dobkin Strategies for stroke rehabilitation , 2004, The Lancet Neurology.

[45]  J. Pineda The functional significance of mu rhythms: Translating “seeing” and “hearing” into “doing” , 2005, Brain Research Reviews.

[46]  Bruno B Averbeck,et al.  Statistical analysis of parieto-frontal cognitive-motor networks. , 2009, Journal of neurophysiology.

[47]  Blake W. Johnson,et al.  Cortical beta oscillations and motor thresholds differ across the spectrum of post-stroke motor impairment, a preliminary MEG and TMS study , 2015, Brain Research.

[48]  D. V. Cramon,et al.  Functional–anatomical concepts of human premotor cortex: evidence from fMRI and PET studies , 2003, NeuroImage.

[49]  Alireza Gharabaghi,et al.  Projecting Navigated TMS Sites on the Gyral Anatomy Decreases Inter-subject Variability of Cortical Motor Maps , 2015, Brain Stimulation.

[50]  C. Braun,et al.  Plasticity of premotor cortico-muscular coherence in severely impaired stroke patients with hand paralysis , 2017, NeuroImage: Clinical.

[51]  C. Richards,et al.  The Kinesthetic and Visual Imagery Questionnaire (KVIQ) for Assessing Motor Imagery in Persons with Physical Disabilities: A Reliability and Construct Validity Study , 2007, Journal of neurologic physical therapy : JNPT.

[52]  Derek Abbott,et al.  Proprioceptive Feedback Facilitates Motor Imagery-Related Operant Learning of Sensorimotor β-Band Modulation , 2017, Front. Neurosci..

[53]  Giacomo Koch,et al.  Focal Stimulation of the Posterior Parietal Cortex Increases the Excitability of the Ipsilateral Motor Cortex , 2007, The Journal of Neuroscience.

[54]  Jonathan R Wolpaw,et al.  Sensorimotor rhythm-based brain–computer interface (BCI): model order selection for autoregressive spectral analysis , 2008, Journal of neural engineering.

[55]  Nick S. Ward,et al.  Do movement-related beta oscillations change after stroke? , 2014, Journal of neurophysiology.

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

[57]  A. Riehle,et al.  The ups and downs of beta oscillations in sensorimotor cortex , 2013, Experimental Neurology.

[58]  A. Gharabaghi,et al.  Self-regulation of circumscribed brain activity modulates spatially selective and frequency specific connectivity of distributed resting state networks , 2015, Front. Behav. Neurosci..

[59]  G. Pfurtscheller,et al.  Could the beta rebound in the EEG be suitable to realize a “brain switch”? , 2009, Clinical Neurophysiology.

[60]  Vincenzo Romei,et al.  Handedness is mainly associated with an asymmetry of corticospinal excitability and not of transcallosal inhibition , 2004, Clinical Neurophysiology.

[61]  Rajesh P. N. Rao,et al.  Cortical activity during motor execution, motor imagery, and imagery-based online feedback , 2010, Proceedings of the National Academy of Sciences.

[62]  Alireza Gharabaghi,et al.  Probing Corticospinal Recruitment Patterns and Functional Synergies with Transcranial Magnetic Stimulation , 2016, Front. Cell. Neurosci..

[63]  Alireza Gharabaghi,et al.  Brain State-Dependent Closed-Loop Modulation of Paired Associative Stimulation Controlled by Sensorimotor Desynchronization , 2016, Front. Cell. Neurosci..

[64]  J. Matias Palva,et al.  Localization of Cortical Phase and Amplitude Dynamics during Visual Working Memory Encoding and Retention , 2011, The Journal of Neuroscience.

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

[66]  Eilon Vaadia,et al.  Neural basis of sensorimotor learning: modifying internal models , 2008, Current Opinion in Neurobiology.

[67]  A. Gharabaghi What Turns Assistive into Restorative Brain-Machine Interfaces? , 2016, Front. Neurosci..

[68]  Rajesh P. N. Rao,et al.  Distributed cortical adaptation during learning of a brain–computer interface task , 2013, Proceedings of the National Academy of Sciences.

[69]  Jill Whitall,et al.  Hand dominance and side of stroke affect rehabilitation in chronic stroke , 2005, Clinical rehabilitation.

[70]  Alireza Gharabaghi,et al.  Brain–robot interface driven plasticity: Distributed modulation of corticospinal excitability , 2016, NeuroImage.

[71]  Michael E. Smith,et al.  Monitoring Task Loading with Multivariate EEG Measures during Complex Forms of Human-Computer Interaction , 2001, Hum. Factors.

[72]  C. Schroeder,et al.  Neuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques , 2008, The Journal of Neuroscience.

[73]  Fred Paas,et al.  When Left Is Not Right , 2013, Psychological science.

[74]  Stuart N Baker,et al.  Synchronization in monkey motor cortex during a precision grip task. II. effect of oscillatory activity on corticospinal output. , 2003, Journal of neurophysiology.

[75]  Alireza Gharabaghi,et al.  Reinforcement learning of self-regulated sensorimotor β-oscillations improves motor performance , 2016, NeuroImage.

[76]  Julien Modolo,et al.  Delayed and lasting effects of deep brain stimulation on locomotion in Parkinson's disease. , 2009, Chaos.

[77]  David J. Nutt,et al.  The effects of elevated endogenous GABA levels on movement-related network oscillations , 2013, NeuroImage.

[78]  Alireza Gharabaghi,et al.  Reinforcement learning of self-regulated β-oscillations for motor restoration in chronic stroke , 2015, Front. Hum. Neurosci..

[79]  Alireza Gharabaghi,et al.  Constraints and Adaptation of Closed-Loop Neuroprosthetics for Functional Restoration , 2017, Front. Neurosci..

[80]  Alireza Gharabaghi,et al.  Brain state-dependent robotic reaching movement with a multi-joint arm exoskeleton: combining brain-machine interfacing and robotic rehabilitation , 2015, Front. Hum. Neurosci..

[81]  Alireza Gharabaghi,et al.  Reinforcement learning for adaptive threshold control of restorative brain-computer interfaces: a Bayesian simulation , 2015, Front. Neurosci..

[82]  J. Nielsen,et al.  Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback , 2007, Nature Neuroscience.

[83]  Wolfgang Rosenstiel,et al.  Coupling brain-machine interfaces with cortical stimulation for brain-state dependent stimulation: enhancing motor cortex excitability for neurorehabilitation , 2014, Front. Hum. Neurosci..

[84]  Nicholas G Hatsopoulos,et al.  Incorporating Feedback from Multiple Sensory Modalities Enhances Brain–Machine Interface Control , 2010, The Journal of Neuroscience.

[85]  M S Gazzaniga,et al.  Anterior and posterior callosal contributions to simultaneous bimanual movements of the hands and fingers. , 2000, Brain : a journal of neurology.

[86]  Mingzhou Ding,et al.  Evaluating causal relations in neural systems: Granger causality, directed transfer function and statistical assessment of significance , 2001, Biological Cybernetics.

[87]  A. Gharabaghi,et al.  Physiological and behavioral effects of β-tACS on brain self-regulation in chronic stroke , 2017, Brain Stimulation.

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

[89]  Alireza Gharabaghi,et al.  Distinct Beta-band Oscillatory Circuits Underlie Corticospinal Gain Modulation , 2018, Cerebral cortex.

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