Investigation of Optimal Afferent Feedback Modality for Inducing Neural Plasticity with A Self-Paced Brain-Computer Interface

Brain-computer interfaces (BCIs) can be used to induce neural plasticity in the human nervous system by pairing motor cortical activity with relevant afferent feedback, which can be used in neurorehabilitation. The aim of this study was to identify the optimal type or combination of afferent feedback modalities to increase cortical excitability in a BCI training intervention. In three experimental sessions, 12 healthy participants imagined a dorsiflexion that was decoded by a BCI which activated relevant afferent feedback: (1) electrical nerve stimulation (ES) (peroneal nerve—innervating tibialis anterior), (2) passive movement (PM) of the ankle joint, or (3) combined electrical stimulation and passive movement (Comb). The cortical excitability was assessed with transcranial magnetic stimulation determining motor evoked potentials (MEPs) in tibialis anterior before, immediately after and 30 min after the BCI training. Linear mixed regression models were used to assess the changes in MEPs. The three interventions led to a significant (p < 0.05) increase in MEP amplitudes immediately and 30 min after the training. The effect sizes of Comb paradigm were larger than ES and PM, although, these differences were not statistically significant (p > 0.05). These results indicate that the timing of movement imagery and afferent feedback is the main determinant of induced cortical plasticity whereas the specific type of feedback has a moderate impact. These findings can be important for the translation of such a BCI protocol to the clinical practice where by combining the BCI with the already available equipment cortical plasticity can be effectively induced. The findings in the current study need to be validated in stroke populations.

[1]  Mads Jochumsen,et al.  Comparison of Features for Movement Prediction from Single-Trial Movement-Related Cortical Potentials in Healthy Subjects and Stroke Patients , 2015, Comput. Intell. Neurosci..

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

[3]  José Luis Pons Rovira,et al.  A Closed-Loop Brain–Computer Interface Triggering an Active Ankle–Foot Orthosis for Inducing Cortical Neural Plasticity , 2014, IEEE Transactions on Biomedical Engineering.

[4]  Mads Jochumsen,et al.  Paired Associative Stimulation Delivered by Pairing Movement‐Related Cortical Potentials With Peripheral Electrical Stimulation: An Investigation of the Duration of Neuromodulatory Effects , 2018, Neuromodulation : journal of the International Neuromodulation Society.

[5]  D. F. Collins,et al.  Central Contributions to Contractions Evoked by Tetanic Neuromuscular Electrical Stimulation , 2007, Exercise and sport sciences reviews.

[6]  Mark E. Dohring,et al.  Feasibility of a New Application of Noninvasive Brain Computer Interface (BCI): A Case Study of Training for Recovery of Volitional Motor Control After Stroke , 2009, Journal of neurologic physical therapy : JNPT.

[7]  D. Farina,et al.  The effect of type of afferent feedback timed with motor imagery on the induction of cortical plasticity , 2017, Brain Research.

[8]  A. Pavlovic,et al.  Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface. , 2016, Journal of neurophysiology.

[9]  Xingyu Wang,et al.  Temporally Constrained Sparse Group Spatial Patterns for Motor Imagery BCI , 2019, IEEE Transactions on Cybernetics.

[10]  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..

[11]  J. Millán,et al.  Brain-actuated functional electrical stimulation elicits lasting arm motor recovery after stroke , 2018, Nature Communications.

[12]  Mads Jochumsen,et al.  Detection and classification of movement-related cortical potentials associated with task force and speed , 2013, Journal of neural engineering.

[13]  Walter Paulus,et al.  The associative brain at work: Evidence from paired associative stimulation studies in humans , 2017, Clinical Neurophysiology.

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

[15]  M. Hallett,et al.  Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. , 1995, Journal of neurophysiology.

[16]  J. Nielsen,et al.  Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man , 2000, The Journal of physiology.

[17]  Xingyu Wang,et al.  Sparse Bayesian Classification of EEG for Brain–Computer Interface , 2016, IEEE Transactions on Neural Networks and Learning Systems.

[18]  G. Lewis,et al.  Short-term Effects of Electrical Stimulation and Voluntary Activity on Corticomotor Excitability in Healthy Individuals and People With Stroke , 2012, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[19]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[20]  Dario Farina,et al.  Detecting and classifying movement-related cortical potentials associated with hand movements in healthy subjects and stroke patients from single-electrode, single-trial EEG , 2015, Journal of neural engineering.

[21]  Thomas Sinkjær,et al.  Cortical excitability changes following grasping exercise augmented with electrical stimulation , 2008, Experimental Brain Research.

[22]  T. Sinkjær,et al.  Evidence that a transcortical pathway contributes to stretch reflexes in the tibialis anterior muscle in man , 1998, The Journal of physiology.

[23]  Mads Jochumsen,et al.  Modeling and Control of Rehabilitation Robotic Device: motoBOTTE , 2018, Converging Clinical and Engineering Research on Neurorehabilitation III.

[24]  Twisk J,et al.  Different ways to estimate treatment effects in randomised controlled trials , 2018, Contemporary clinical trials communications.

[25]  Ning Jiang,et al.  Peripheral Electrical Stimulation Triggered by Self-Paced Detection of Motor Intention Enhances Motor Evoked Potentials , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[26]  Ning Jiang,et al.  Enhanced Low-Latency Detection of Motor Intention From EEG for Closed-Loop Brain-Computer Interface Applications , 2014, IEEE Transactions on Biomedical Engineering.

[27]  John C Rothwell,et al.  Differences between the effects of three plasticity inducing protocols on the organization of the human motor cortex , 2006, The European journal of neuroscience.

[28]  D. Farina,et al.  Detection of movement intention from single-trial movement-related cortical potentials , 2011, Journal of neural engineering.

[29]  José del R. Millán,et al.  Sensory threshold neuromuscular electrical stimulation fosters motor imagery performance , 2018, NeuroImage.

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

[31]  L. Cohen,et al.  Induction of plasticity in the human motor cortex by paired associative stimulation. , 2000, Brain : a journal of neurology.

[32]  Tim Friede,et al.  Blinded versus unblinded estimation of a correlation coefficient to inform interim design adaptations , 2016, Biometrical journal. Biometrische Zeitschrift.

[33]  J L Pons,et al.  Detection of the onset of upper-limb movements based on the combined analysis of changes in the sensorimotor rhythms and slow cortical potentials , 2014, Journal of neural engineering.

[34]  Sjoerd J de Vries,et al.  Motor imagery and stroke rehabilitation: a critical discussion. , 2007, Journal of rehabilitation medicine.

[35]  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.

[36]  D. Farina,et al.  Precise temporal association between cortical potentials evoked by motor imagination and afference induces cortical plasticity , 2012, The Journal of physiology.

[37]  E. Biryukova,et al.  Post-stroke Rehabilitation Training with a Motor-Imagery-Based Brain-Computer Interface (BCI)-Controlled Hand Exoskeleton: A Randomized Controlled Multicenter Trial , 2017, Front. Neurosci..

[38]  Gernot R Müller-Putz,et al.  Upper limb movements can be decoded from the time-domain of low-frequency EEG , 2017, PloS one.

[39]  D. F. Collins,et al.  Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: triceps surae. , 2011, Journal of applied physiology.

[40]  Mads Jochumsen,et al.  Pairing Voluntary Movement and Muscle-Located Electrical Stimulation Increases Cortical Excitability , 2016, Front. Hum. Neurosci..

[41]  M. Ridding,et al.  Determinants of the induction of cortical plasticity by non‐invasive brain stimulation in healthy subjects , 2010, The Journal of physiology.

[42]  Ning Jiang,et al.  Detection of Movement Related Cortical Potentials from EEG Using Constrained ICA for Brain-Computer Interface Applications , 2017, Front. Neurosci..

[43]  Cuntai Guan,et al.  Brain-Computer Interface in Stroke Rehabilitation , 2013, J. Comput. Sci. Eng..

[44]  Yu Zhang,et al.  EEG classification using sparse Bayesian extreme learning machine for brain–computer interface , 2018, Neural Computing and Applications.

[45]  J. Millán,et al.  Detection of self-paced reaching movement intention from EEG signals , 2012, Front. Neuroeng..

[46]  H. Asanuma,et al.  Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. , 1993, Journal of neurophysiology.

[47]  Tomohiro Kizuka,et al.  Motor imagery and electrical stimulation reproduce corticospinal excitability at levels similar to voluntary muscle contraction , 2014, Journal of NeuroEngineering and Rehabilitation.

[48]  T Sinkjaer,et al.  Changes in excitability of the cortical projections to the human tibialis anterior after paired associative stimulation. , 2007, Journal of neurophysiology.

[49]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[50]  Fumitoshi Matsuno,et al.  A Novel EOG/EEG Hybrid Human–Machine Interface Adopting Eye Movements and ERPs: Application to Robot Control , 2015, IEEE Transactions on Biomedical Engineering.

[51]  J.-F. Debril,et al.  Enhanced precision of ankle torque measure with an open-unit dynamometer mounted with a 3D force-torque sensor , 2015, European Journal of Applied Physiology.

[52]  Mads Jochumsen,et al.  Effect of subject training on a movement-related cortical potential-based brain-computer interface , 2018, Biomed. Signal Process. Control..

[53]  J. Nielsen,et al.  Afferent feedback in the control of human gait. , 2002, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[54]  Thomas Sinkjaer,et al.  Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive , 2005, Experimental Brain Research.