Backward Walking Induces Significantly Larger Upper-Mu-Rhythm Suppression Effects Than Forward Walking Does

Studies have compared the differences and similarities between backward walking and forward walking, and demonstrated the potential of backward walking for gait rehabilitation. However, current evidence supporting the benefits of backward walking over forward walking remains inconclusive. Considering the proven association between gait and the cerebral cortex, we used electroencephalograms (EEG) to differentiate the effects of backward walking and forward walking on cortical activities, by comparing the sensorimotor rhythm (8–12 Hz, also called mu rhythm) of EEG signals. A systematic signal procedure was used to eliminate the motion artifacts induced by walking to safeguard EEG signal fidelity. Statistical test results of our experimental data demonstrated that walking motions significantly suppressed mu rhythm. Moreover, backward walking exhibited significantly larger upper mu rhythm (10–12 Hz) suppression effects than forward walking did. This finding implies that backward walking induces more sensorimotor cortex activity than forward walking does, and provides a basis to support the potential benefits of backward walking over forward walking. By monitoring the upper mu rhythm throughout the rehabilitation process, medical experts can adaptively adjust the intensity and duration of each walking training session to improve the efficacy of a walking ability recovery program.

[1]  Tony W. Wilson,et al.  Stride-time variability and sensorimotor cortical activation during walking , 2012, NeuroImage.

[2]  F. Lacquaniti,et al.  Motor patterns for human gait: backward versus forward locomotion. , 1998, Journal of neurophysiology.

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

[4]  J. Rothwell,et al.  Endogenous control of waking brain rhythms induces neuroplasticity in humans , 2010, The European journal of neuroscience.

[5]  T. Komiyama,et al.  Circuit Mechanisms of Sensorimotor Learning , 2016, Neuron.

[6]  Francesca Figliozzi,et al.  Detecting temporal reversals in human locomotion , 2011, Experimental Brain Research.

[7]  I. Tseng,et al.  Comparisons of forward and backward gait between poorer and better attention capabilities in early Parkinson's disease. , 2012, Gait & posture.

[8]  G. Cheron,et al.  Oscillations in the human brain during walking execution, imagination and observation , 2015, Neuropsychologia.

[9]  Daniel P. Ferris,et al.  Independent Component Analysis of Gait-Related Movement Artifact Recorded using EEG Electrodes during Treadmill Walking , 2015, Front. Hum. Neurosci..

[10]  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.

[11]  Tele Tan,et al.  3D visualization of movements can amplify motor cortex activation during subsequent motor imagery , 2015, Front. Hum. Neurosci..

[12]  Clemens Brunner,et al.  Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks , 2006, NeuroImage.

[13]  Daniel P Ferris,et al.  Restricted vision increases sensorimotor cortex involvement in human walking. , 2017, Journal of neurophysiology.

[14]  M. Erb,et al.  Activation of Cortical and Cerebellar Motor Areas during Executed and Imagined Hand Movements: An fMRI Study , 1999, Journal of Cognitive Neuroscience.

[15]  Usman Rashid,et al.  An EEG Experimental Study Evaluating the Performance of Texas Instruments ADS1299 , 2018, Sensors.

[16]  Christa Neuper,et al.  Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able-bodied subjects , 2012, NeuroImage.

[17]  Deepak Nagaria,et al.  LMS Adaptive Filters for Noise Cancellation: A Review , 2017 .

[18]  S. Small,et al.  Fine modulation in network activation during motor execution and motor imagery. , 2004, Cerebral cortex.

[19]  A. Mark Williams,et al.  The role of cortical sensorimotor oscillations in action anticipation , 2017, NeuroImage.

[20]  S. Kachanathu,et al.  Efficacy of backward versus forward walking on hamstring strain rehabilitation , 2013 .

[21]  W. Klimesch Memory processes, brain oscillations and EEG synchronization. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  Gernot R. Müller-Putz,et al.  High and low gamma EEG oscillations in central sensorimotor areas are conversely modulated during the human gait cycle , 2015, NeuroImage.

[23]  C. Neuper,et al.  Upper Alpha Based Neurofeedback Training in Chronic Stroke: Brain Plasticity Processes and Cognitive Effects , 2017, Applied Psychophysiology and Biofeedback.

[24]  R. An,et al.  Effectiveness of backward walking training on balance performance: A systematic review and meta-analysis. , 2019, Gait & posture.

[25]  Amir Rastegarnia,et al.  Methods for artifact detection and removal from scalp EEG: A review , 2016, Neurophysiologie Clinique/Clinical Neurophysiology.

[26]  Tanja Schultz,et al.  Mechanisms within the Parietal Cortex Correlate with the Benefits of Random Practice in Motor Adaptation , 2017, Front. Hum. Neurosci..

[27]  V. Brümmer,et al.  Primary motor cortex activity is elevated with incremental exercise intensity , 2011, Neuroscience.

[28]  Yu Liu,et al.  Simultaneous ocular and muscle artifact removal from EEG data by exploiting diverse statistics , 2017, Comput. Biol. Medicine.

[29]  Simanto Saha,et al.  Intra- and Inter-subject Variability in EEG-Based Sensorimotor Brain Computer Interface: A Review , 2020, Frontiers in Computational Neuroscience.

[30]  M. Smutok,et al.  Comparison of cardiopulmonary responses to forward and backward walking and running. , 1994, Medicine and science in sports and exercise.

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

[32]  E. Chaloupka,et al.  Cardiorespiratory and metabolic responses during forward and backward walking. , 1997, The Journal of orthopaedic and sports physical therapy.

[33]  Kimberly Milla,et al.  Does Movement Matter? Prefrontal Cortex Activity During 2D vs. 3D Performance of the Tower of Hanoi Puzzle , 2019, Front. Hum. Neurosci..

[34]  T. Ros,et al.  Neurofeedback facilitation of implicit motor learning , 2014, Biological Psychology.

[35]  Roland R. Lee,et al.  Temporal dynamics of ipsilateral and contralateral motor activity during voluntary finger movement , 2004, Human brain mapping.

[36]  T. Drew,et al.  Taking the next step: cortical contributions to the control of locomotion , 2015, Current Opinion in Neurobiology.

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

[38]  J. Ushiba,et al.  Ipsilateral EEG mu rhythm reflects the excitability of uncrossed pathways projecting to shoulder muscles , 2017, Journal of NeuroEngineering and Rehabilitation.

[39]  G. Pfurtscheller,et al.  Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement , 2000, Clinical Neurophysiology.

[40]  Daniel P. Ferris,et al.  Electrocortical activity is coupled to gait cycle phase during treadmill walking , 2011, NeuroImage.

[41]  Kathryn H. Yoo,et al.  Assessing human mirror activity with EEG mu rhythm: A meta-analysis. , 2016, Psychological bulletin.

[42]  Daniel Hamacher,et al.  Brain activity during walking: A systematic review , 2015, Neuroscience & Biobehavioral Reviews.

[43]  Daniel P Ferris,et al.  Faster gait speeds reduce alpha and beta EEG spectral power from human sensorimotor cortex , 2019, IEEE Transactions on Biomedical Engineering.

[44]  M. Kim,et al.  Therapeutic efficacy of walking backward and forward on a slope in normal adults , 2016, Journal of physical therapy science.

[45]  P. Celnik,et al.  Stroke Rehabilitation. , 2015, Physical medicine and rehabilitation clinics of North America.

[46]  J. Lange,et al.  Event-related desynchronization of mu and beta oscillations during the processing of novel tool names , 2018, Brain and Language.

[47]  Matt Stead,et al.  Human Neuroscience , 2022 .

[48]  Christa Neuper,et al.  Distinct β Band Oscillatory Networks Subserving Motor and Cognitive Control during Gait Adaptation , 2016, The Journal of Neuroscience.

[49]  H. Dinse,et al.  Repetitive tactile stimulation changes resting-state functional connectivity—implications for treatment of sensorimotor decline , 2012, Front. Hum. Neurosci..

[50]  Kaat Desloovere,et al.  Interlimb Coordination during Forward and Backward Walking in Primary School-Aged Children , 2013, PloS one.

[51]  D. Ostry,et al.  Sensory Plasticity in Human Motor Learning , 2016, Trends in Neurosciences.

[52]  S. Kachanathu,et al.  Effect of Forward and Backward Locomotion Training on Anaerobic Performance and Anthropometrical Composition , 2014, Journal of physical therapy science.

[53]  Daniel P. Ferris,et al.  Removal of movement artifact from high-density EEG recorded during walking and running. , 2010, Journal of neurophysiology.

[54]  Gui-Bin Bian,et al.  Removal of Artifacts from EEG Signals: A Review , 2019, Sensors.

[55]  Three-dimensional Motion Analysis of the Ankle during Backward Walking , 2013, Journal of physical therapy science.

[56]  A. Fast,et al.  One step forward and two steps back: the dangers of walking backwards in therapy. , 2000, American journal of physical medicine & rehabilitation.

[57]  Silvia Comani,et al.  Monitoring Neuro-Motor Recovery From Stroke With High-Resolution EEG, Robotics and Virtual Reality: A Proof of Concept , 2015, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[58]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[59]  H. Fukuyama,et al.  Alpha-band desynchronization in human parietal area during reach planning , 2012, Clinical Neurophysiology.

[60]  J. F. Yang,et al.  Backward walking: a simple reversal of forward walking? , 1989, Journal of motor behavior.

[61]  A. Harel,et al.  Investigating Neural Sensorimotor Mechanisms Underlying Flight Expertise in Pilots: Preliminary Data From an EEG Study , 2018, Front. Hum. Neurosci..

[62]  J. Kropotov Quantitative EEG, Event-Related Potentials and Neurotherapy , 2008 .

[63]  N. Takeuchi,et al.  Rehabilitation with Poststroke Motor Recovery: A Review with a Focus on Neural Plasticity , 2013, Stroke research and treatment.

[64]  Sylvie Nadeau,et al.  Head and trunk stabilization strategies during forward and backward walking in healthy adults. , 2003, Gait & Posture.

[65]  E. Basar A review of alpha activity in integrative brain function: fundamental physiology, sensory coding, cognition and pathology. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[66]  Max J Kurz,et al.  Neurophysiological abnormalities in the sensorimotor cortices during the motor planning and movement execution stages of children with cerebral palsy , 2014, Developmental medicine and child neurology.

[67]  M. Dinomais,et al.  Mu rhythm: state of the art with special focus on cerebral palsy. , 2020, Annals of physical and rehabilitation medicine.

[68]  T G Deliagina,et al.  Activity of motor cortex neurons during backward locomotion. , 2011, Journal of neurophysiology.

[69]  Dietmar Saupe,et al.  Bicycling and Walking are Associated with Different Cortical Oscillatory Dynamics , 2016, Front. Hum. Neurosci..

[70]  W. David Hairston,et al.  Human electrocortical dynamics while stepping over obstacles , 2019, Scientific Reports.

[71]  Daniel P Ferris,et al.  Isolating gait-related movement artifacts in electroencephalography during human walking , 2015, Journal of neural engineering.

[72]  Rong Song,et al.  Developing a Low-Cost Force Treadmill via Dynamic Modeling , 2017, Journal of healthcare engineering.

[73]  Theresa E. McGuirk,et al.  Prefrontal over-activation during walking in people with mobility deficits: Interpretation and functional implications. , 2018, Human movement science.

[74]  G. Pfurtscheller,et al.  Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[75]  Daniel P. Ferris,et al.  Visual Evoked Responses During Standing and Walking , 2010, Front. Hum. Neurosci..

[76]  Ruopeng An,et al.  Effectiveness of backward walking training on spatial-temporal gait characteristics: A systematic review and meta-analysis. , 2018, Human movement science.

[77]  Shorouk Elshennawy,et al.  Effects of backward gait training on balance, gross motor function, and gait in children with cerebral palsy: a systematic review , 2018, Clinical rehabilitation.

[78]  E. Eichler,et al.  Exploring the heterogeneity of neural social indices for genetically distinct etiologies of autism , 2017, Journal of Neurodevelopmental Disorders.

[79]  Daniel P Ferris,et al.  Dual-electrode motion artifact cancellation for mobile electroencephalography , 2018, Journal of neural engineering.

[80]  M. Ding,et al.  Amplitude of Sensorimotor Mu Rhythm Is Correlated with BOLD from Multiple Brain Regions: A Simultaneous EEG-fMRI Study , 2016, Front. Hum. Neurosci..

[81]  Tharani Balasukumaran,et al.  The effectiveness of backward walking as a treatment for people with gait impairments: a systematic review and meta-analysis , 2018, Clinical rehabilitation.

[82]  A. Hall,et al.  Adaptive Switching Circuits , 2016 .

[83]  Y. Kim,et al.  Assessment of Cognitive Engagement in Stroke Patients From Single-Trial EEG During Motor Rehabilitation , 2015, IEEE Transactions on Neural Systems and Rehabilitation Engineering.