Synchronous EMG Activity in the Piper Frequency Band Reveals the Corticospinal Demand of Walking Tasks

Evidence indicates that the frequency-domain characteristics of surface electromyogram (EMG) signals are modulated according to the contributing sources of neural drive. Modulation of inter-muscular EMG synchrony within the Piper frequency band (30–60 Hz) during movement tasks has been linked to drive from the corticospinal tract. However, it is not known whether EMG synchrony is sufficiently sensitive to detect task-dependent differences in the corticospinal contribution to leg muscle activation during walking. We investigated this question in seventeen healthy older men and women. It was hypothesized that, relative to typical steady state walking, Piper band EMG synchrony of the triceps surae muscle group would be reduced for dual-task walking (because of competition for cortical resources), similar for fast walking (because walking speed is directed by an indirect locomotor pathway rather than by the corticospinal tract), and increased when taking a long step (because voluntary gait pattern modifications are directed by the corticospinal tract). Each of these hypotheses was confirmed. These findings support the use of frequency-domain analysis of EMG in future investigations into the corticospinal contribution to control of healthy and disordered human walking.

[1]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Gorassini,et al.  Changes in cortically related intermuscular coherence accompanying improvements in locomotor skills in incomplete spinal cord injury. , 2006, Journal of neurophysiology.

[3]  J. Nielsen,et al.  Reduction of common synaptic drive to ankle dorsiflexor motoneurons during walking in patients with spinal cord lesion. , 2005, Journal of neurophysiology.

[4]  Marie-Claude Hepp-Reymond,et al.  Gamma-range corticomuscular coherence during dynamic force output , 2007, NeuroImage.

[5]  B. Conway,et al.  Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. , 1995, The Journal of physiology.

[6]  B. Conway,et al.  The motor cortex drives the muscles during walking in human subjects , 2012, The Journal of physiology.

[7]  Jean Pailhous,et al.  Intentional on-line adaptation of stride length in human walking , 1999, Experimental Brain Research.

[8]  R. Lemon,et al.  Human Cortical Muscle Coherence Is Directly Related to Specific Motor Parameters , 2000, The Journal of Neuroscience.

[9]  Otmar Bock,et al.  Dual-task costs while walking increase in old age for some, but not for other tasks: an experimental study of healthy young and elderly persons , 2008, Journal of NeuroEngineering and Rehabilitation.

[10]  Dario Farina,et al.  Interpretation of the Surface Electromyogram in Dynamic Contractions , 2006, Exercise and sport sciences reviews.

[11]  R. Kristeva-Feige,et al.  Effects of attention and precision of exerted force on beta range EEG-EMG synchronization during a maintained motor contraction task , 2002, Clinical Neurophysiology.

[12]  Zoran Cvetkovic,et al.  Rectification of the EMG is an unnecessary and inappropriate step in the calculation of Corticomuscular coherence , 2012, Journal of Neuroscience Methods.

[13]  E. Olivier,et al.  Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation , 1997, The Journal of physiology.

[14]  J. Nielsen,et al.  Reduction of common motoneuronal drive on the affected side during walking in hemiplegic stroke patients , 2008, Clinical Neurophysiology.

[15]  Joseph T. Gwin,et al.  Motor control and aging: Links to age-related brain structural, functional, and biochemical effects , 2010, Neuroscience & Biobehavioral Reviews.

[16]  Gary Kamen,et al.  Essentials of Electromyography , 2009 .

[17]  E. Delagi,et al.  Anatomical guide for the electromyographer : the limbs and trunk /by Edward F. Delagi [et al.] ; illustrated by Phyllis B. Hammond, Aldo O. Perotto, and Hugh Thomas , 2005 .

[18]  A. Curt,et al.  Voluntary control of human gait: conditioning of magnetically evoked motor responses in a precision stepping task , 1999, Experimental Brain Research.

[19]  Minoru Shinohara,et al.  Attenuation of corticomuscular coherence with additional motor or non-motor task , 2011, Clinical Neurophysiology.

[20]  Ichiro Miyai,et al.  Activities in the frontal cortex and gait performance are modulated by preparation. An fNIRS study , 2008, NeuroImage.

[21]  Chris Rorden,et al.  Lesion Mapping of Cognitive Abilities Linked to Intelligence , 2009, Neuron.

[22]  Aslak Grinsted,et al.  Nonlinear Processes in Geophysics Application of the Cross Wavelet Transform and Wavelet Coherence to Geophysical Time Series , 2022 .

[23]  Bernard A Conway,et al.  Impaired transmission in the corticospinal tract and gait disability in spinal cord injured persons. , 2010, Journal of neurophysiology.

[24]  E. Christou,et al.  Increased voluntary drive is associated with changes in common oscillations from 13 to 60 Hz of interference but not rectified electromyography , 2010, Muscle & nerve.

[25]  B. Bussel,et al.  Evidence for Cognitive Processes Involved in the Control of Steady State of Walking in Healthy Subjects and after Cerebral Damage , 2005, Neurorehabilitation and neural repair.

[26]  Carlo J. De Luca,et al.  The Use of Surface Electromyography in Biomechanics , 1997 .

[27]  P. Brown,et al.  EEG–EMG, MEG–EMG and EMG–EMG frequency analysis: physiological principles and clinical applications , 2002, Clinical Neurophysiology.

[28]  T. Drew,et al.  Motor cortical cell discharge during voluntary gait modification , 1988, Brain Research.

[29]  P. de Leva Adjustments to Zatsiorsky-Seluyanov's segment inertia parameters. , 1996, Journal of biomechanics.

[30]  J. Nielsen,et al.  Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking , 2001, The Journal of physiology.

[31]  E. Christou,et al.  Identification of Oscillations in Muscle Activity From Surface EMG: Reply to Halliday and Farmer , 2010 .

[32]  J. R. Rosenberg,et al.  Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans , 1998, Neuroscience Letters.

[33]  M. Bonnard,et al.  Task‐induced modulation of motor evoked potentials in upper‐leg muscles during human gait: a TMS study , 2002, The European journal of neuroscience.

[34]  R. Hari,et al.  Cortical control of human motoneuron firing during isometric contraction. , 1997, Journal of neurophysiology.

[35]  V. Jousmäki,et al.  Task‐dependent modulation of 15‐30 Hz coherence between rectified EMGs from human hand and forearm muscles , 1999, The Journal of physiology.

[36]  William H. Gage,et al.  The allocation of attention during locomotion is altered by anxiety , 2003, Experimental Brain Research.

[37]  J. Nielsen,et al.  Childhood development of common drive to a human leg muscle during ankle dorsiflexion and gait , 2010, The Journal of physiology.

[38]  M. Molinari,et al.  Rehabilitation of gait after stroke: a review towards a top-down approach , 2011, Journal of NeuroEngineering and Rehabilitation.

[39]  Reply to Boonstra: The Nature of Periodic Input to the Muscle. , 2010 .

[40]  S. Grillner,et al.  Neural bases of goal-directed locomotion in vertebrates—An overview , 2008, Brain Research Reviews.

[41]  Trevor Drew,et al.  Locomotor role of the corticoreticular-reticulospinal-spinal interneuronal system. , 2004, Progress in brain research.

[42]  F. E. Delagi Anatomical guide for the electromyographer , 2014 .

[43]  Osmar Pinto Neto,et al.  Rectification of the EMG signal impairs the identification of oscillatory input to the muscle. , 2010, Journal of neurophysiology.

[44]  A. Curt,et al.  Corticospinal input in human gait: modulation of magnetically evoked motor responses , 1997, Experimental Brain Research.

[45]  P. Brown Cortical drives to human muscle: the Piper and related rhythms , 2000, Progress in Neurobiology.

[46]  J. Rothwell,et al.  Cortical correlate of the Piper rhythm in humans. , 1998, Journal of neurophysiology.

[47]  D. Armstrong,et al.  Changes in the discharge patterns of motor cortical neurones associated with volitional changes in stepping in the cat , 1990, Neuroscience Letters.

[48]  Roberto Merletti,et al.  The extraction of neural strategies from the surface EMG. , 2004, Journal of applied physiology.

[49]  M. Sirota,et al.  Differences in movement mechanics, electromyographic, and motor cortex activity between accurate and nonaccurate stepping. , 2010, Journal of neurophysiology.

[50]  C. Torrence,et al.  A Practical Guide to Wavelet Analysis. , 1998 .

[51]  J. Nielsen How we Walk: Central Control of Muscle Activity during Human Walking , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.