Neurophysiological Correlates of Gait Retraining With Real-Time Visual and Auditory Feedback

Most people acquire motor skills through feedback-based training. How the human brain processes sensory feedbacks during training, especially in a gait training, remain largely unclear. The purpose of this paper is to explore how humans adopt a new gait pattern to reduce impacts during walking-with the aid of visual and audio feedbacks. This paper demonstrates the features of underlying brain activity in incorporating the visual or auditory cues to acquire a new gait pattern. Electroencephalography (EEG) and peak positive acceleration (PPA) of the heel were collected from 23 participants during walking on a treadmill with no feedback, with visual feedback, or with audio feedback. The feedbacks were presented after each foot strike, where a sub-threshold PPA triggered a positive feedback (green/low-pitched), and a suprathreshold PPA triggered a negative feedback (red/high-pitched). The participants were instructed to voluntarily control their gait, so that low PPA could be achieved. This control was perturbed in some sessions by an additional cognitive task, and the influence of such distraction was also explored. The PPA was significantly lower in the sessions with visual or audio feedback than in sessions without feedback, showing an immediate improvement in gait pattern, when the feedback was provided. Different feedbacks modulated neural activities at different locations and/or levels during training. Alpha event-related synchronization (ERS) was particularly increased during the encoding of auditory feedback or the introduction of a distracting task. In the meantime, prominent frontal and posterior theta ERS were coupled with negative feedback, and strong beta event-related desynchronization (ERD) was observed only in sessions with feedbacks. Our results indicate that feedback effectively enhances motor planning when acquiring a new gait.

[1]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[2]  C. Y. Leung,et al.  Measurement agreement between a newly developed sensing insole and traditional laboratory-based method for footstrike pattern detection in runners , 2017, PloS one.

[3]  Clare E. Milner,et al.  Reducing Impact Loading in Runners: A One-Year Follow-up , 2018, Medicine and science in sports and exercise.

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

[5]  Z. Y. Chan,et al.  Immediate effects of modified landing pattern on a probabilistic tibial stress fracture model in runners. , 2016, Clinical biomechanics.

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

[7]  Matti Laine,et al.  Cortical activation related to auditory semantic matching of concrete versus abstract words , 1999, Clinical Neurophysiology.

[8]  Giuseppe Pellizzer,et al.  Brain oscillatory activity during motor preparation: effect of directional uncertainty on beta, but not alpha, frequency band , 2015, Front. Neurosci..

[9]  H. P. Crowell,et al.  Gait retraining to reduce lower extremity loading in runners. , 2011, Clinical biomechanics.

[10]  W. Klimesch.  Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[11]  Antonio Cerasa,et al.  Walking indoors, walking outdoors: an fMRI study , 2015, Front. Psychol..

[12]  Daniel P. Ferris,et al.  Beta- and gamma-range human lower limb corticomuscular coherence , 2012, Front. Hum. Neurosci..

[13]  Allison M Brown,et al.  Gait Retraining for Injured and Healthy Runners Using Augmented Feedback: A Systematic Literature Review. , 2015, The Journal of orthopaedic and sports physical therapy.

[14]  Kenneth Kreutz-Delgado,et al.  Super-Gaussian Mixture Source Model for ICA , 2006, ICA.

[15]  Zoe Y S Chan,et al.  Impact Loading During Distracted Running Before and After Auditory Gait Retraining , 2018, International Journal of Sports Medicine.

[16]  M. Laine,et al.  Event-related desynchronization and synchronization during an auditory lexical matching task. , 1998, Electroencephalography and clinical neurophysiology.

[17]  F. H. Lopes da Silva.  EEG and MEG: relevance to neuroscience. , 2013, Neuron.

[18]  Hyung-Soon Park,et al.  Prefrontal, posterior parietal and sensorimotor network activity underlying speed control during walking , 2015, Front. Hum. Neurosci..

[19]  Simon Grondin,et al.  About optimal timing and stability of Weber fraction for duration discrimination , 2001 .

[20]  D. Serrien.  Verbal–manual interactions during dual task performance: An EEG study , 2009, Neuropsychologia.

[21]  I. Davis,et al.  Comparison of lower extremity kinematic curves during overground and treadmill running. , 2010, Journal of applied biomechanics.

[22]  L. D. Goodfellow,et al.  An Empirical Comparison of Audition, Vision, and Touch in the Discrimination of Short Intervals of Time , 1934 .

[23]  Daniel P. Ferris,et al.  An EEG-based study of discrete isometric and isotonic human lower limb muscle contractions , 2012, Journal of NeuroEngineering and Rehabilitation.

[24]  Wolfgang Klimesch,et al.  Alpha Oscillations and Early Stages of Visual Encoding , 2011, Front. Psychology.

[25]  C. Neuper,et al.  It's how you get there: walking down a virtual alley activates premotor and parietal areas , 2014, Front. Hum. Neurosci..

[26]  Christina M Krause,et al.  Cognition- and memory-related ERD/ERS responses in the auditory stimulus modality. , 2006, Progress in brain research.

[27]  Loredana Zollo,et al.  Brain activity preceding a 2D manual catching task , 2009, NeuroImage.

[28]  J. Doyon,et al.  Contributions of the basal ganglia and functionally related brain structures to motor learning , 2009, Behavioural Brain Research.

[29]  S. Olney,et al.  Feedback of ankle joint angle and soleus electromyography in the rehabilitation of hemiplegic gait. , 1993, Archives of physical medicine and rehabilitation.

[30]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[31]  Leslie G. Ungerleider,et al.  Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning , 2003, Neuropsychologia.

[32]  Yoram Baram,et al.  Gait improvement in patients with cerebral palsy by visual and auditory feedback , 2009 .

[33]  Thomas Brochier,et al.  Modulations of EEG Beta Power during Planning and Execution of Grasping Movements , 2013, PloS one.

[34]  Giulio Tononi,et al.  Modulation of Gamma and Theta Spectral Amplitude and Phase Synchronization Is Associated with the Development of Visuo-Motor Learning , 2011, The Journal of Neuroscience.

[35]  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.

[36]  Zoe Y. S. Chan,et al.  Immediate and short-term effects of gait retraining on the knee joint moments and symptoms in patients with early tibiofemoral joint osteoarthritis: a randomized controlled trial. , 2018, Osteoarthritis and cartilage.

[37]  Christian Haarala Björnberg,et al.  Brain oscillatory 1–30Hz EEG ERD/ERS responses during the different stages of an auditory memory search task , 2006, Neuroscience Letters.

[38]  Simon Grondin,et al.  Duration discrimination of empty and filled intervals marked by auditory and visual signals , 1993, Perception & psychophysics.

[39]  Bhaskar D. Rao,et al.  Newton method for the ICA mixture model , 2008, 2008 IEEE International Conference on Acoustics, Speech and Signal Processing.

[40]  W. Klimesch,et al.  The role of theta and alpha oscillations for language comprehension in the human electroencephalogram , 2001, Neuroscience Letters.

[41]  G. Vingerhoets,et al.  Functional connectivity associated with hand shape generation: Imitating novel hand postures and pantomiming tool grips challenge different nodes of a shared neural network , 2015, Human brain mapping.

[42]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[43]  G Pfurtscheller,et al.  Graphical display and statistical evaluation of event-related desynchronization (ERD). , 1977, Electroencephalography and clinical neurophysiology.

[44]  Caroline Di Bernardi Luft,et al.  Learning from feedback: The neural mechanisms of feedback processing facilitating better performance , 2014, Behavioural Brain Research.

[45]  A. Leuthold,et al.  Beta-Band Activity during Motor Planning Reflects Response Uncertainty , 2010, The Journal of Neuroscience.

[46]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[47]  K. Aminian,et al.  Stride-to-stride variability while enumerating animal names among healthy young adults: result of stride velocity or effect of attention-demanding task? , 2008, Gait & posture.

[48]  Rodolphe J. Gentili,et al.  Cortical network modeling for inverse kinematic computation of an anthropomorphic finger , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[49]  G. Borm,et al.  The effect of cognitive dual tasks on balance during walking in physically fit elderly people. , 2007, Archives of physical medicine and rehabilitation.

[50]  Hee Kyung Park,et al.  The Effects of Visual and Auditory Cues on Freezing of Gait in Patients with Parkinson Disease , 2012, American journal of physical medicine & rehabilitation.

[51]  G. Pfurtscheller,et al.  Event-related cortical desynchronization detected by power measurements of scalp EEG. , 1977, Electroencephalography and clinical neurophysiology.

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

[53]  Zoe Y. S. Chan,et al.  Gait Retraining for the Reduction of Injury Occurrence in Novice Distance Runners: 1-Year Follow-up of a Randomized Controlled Trial , 2018, The American journal of sports medicine.

[54]  F. Macar,et al.  Sensory effects on judgments of short time-intervals , 1998, Psychological research.

[55]  Kurt A. Thoroughman,et al.  Divided attention impairs human motor adaptation but not feedback control. , 2007, Journal of neurophysiology.

[56]  Zoe Y S Chan,et al.  Control of impact loading during distracted running before and after gait retraining in runners , 2018, Journal of sports sciences.

[57]  Junichi Ushiba,et al.  The comparison of motor learning performance with and without feedback , 2012, Somatosensory & motor research.

[58]  M. Suteerawattananon,et al.  Effects of visual and auditory cues on gait in individuals with Parkinson's disease , 2004, Journal of the Neurological Sciences.

[59]  Daniel P Ferris,et al.  Walking reduces sensorimotor network connectivity compared to standing , 2014, Journal of NeuroEngineering and Rehabilitation.