Abstract
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.
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Amos, A., D. M. Armstrong, and D. E. Marple-Horvat. Changes in the discharge patterns of motor cortical neurones associated with volitional changes in stepping in the cat. Neurosci. Lett. 109:107–112, 1990.
Baker, S. N., E. Olivier, and R. N. Lemon. Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J. Physiol. 501(Pt 1):225–241, 1997.
Barthelemy, D., M. Willerslev-Olsen, H. Lundell, B. A. Conway, H. Knudsen, F. Biering-Sorensen, and J. B. Nielsen. Impaired transmission in the corticospinal tract and gait disability in spinal cord injured persons. J. Neurophysiol. 104:1167–1176, 2010.
Belda-Lois, J. M., S. Mena-del Horno, I. Bermejo-Bosch, J. C. Moreno, J. L. Pons, D. Farina, M. Iosa, M. Molinari, F. Tamburella, A. Ramos, A. Caria, T. Solis-Escalante, C. Brunner, and M. Rea. Rehabilitation of gait after stroke: a review towards a top-down approach. J. Neuroeng. Rehabil. 8:66, 2011.
Beloozerova, I. N., B. J. Farrell, M. G. Sirota, and B. I. Prilutsky. Differences in movement mechanics, electromyographic, and motor cortex activity between accurate and non-accurate stepping. J. Neurophysiol. 103(4):2285–2300, 2010.
Bock, O. 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. J. Neuroeng. Rehabil. 5:27, 2008.
Bonnard, M., M. Camus, T. Coyle, and J. Pailhous. Task-induced modulation of motor evoked potentials in upper-leg muscles during human gait: a TMS study. Eur. J. Neurosci. 16:2225–2230, 2002.
Brown, P. Cortical drives to human muscle: the Piper and related rhythms. Prog. Neurobiol. 60:97–108, 2000.
Brown, P., S. Salenius, J. C. Rothwell, and R. Hari. Cortical correlate of the Piper rhythm in humans. J. Neurophysiol. 80:2911–2917, 1998.
Christou, E. A., and O. P. Neto. Identification of oscillations in muscle activity from surface EMG: reply to Halliday and Farmer. J. Neurophysiol. 103:3548–3549, 2010.
Christou, E. A., and O. P. Neto. Reply to Boonstra: the nature of periodic input to the muscle. J. Neurophysiol. 104:577, 2010.
Conway, B. A., D. M. Halliday, S. F. Farmer, U. Shahani, P. Maas, A. I. Weir, and J. R. Rosenberg. Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J. Physiol. 489(Pt 3):917–924, 1995.
de Leva, P. Adjustments to Zatsiorsky-Seluyanov’s segment inertia parameters. J. Biomech. 29:1223–1230, 1996.
De Luca, C. J. The use of surface electromyography in biomechanics. J. Appl. Biomech. 13:135–163, 1997.
Drew, T. Motor cortical cell discharge during voluntary gait modification. Brain Res. 457:181–187, 1988.
Farina, D. Interpretation of the surface electromyogram in dynamic contractions. Exerc. Sport Sci. Rev. 34:121–127, 2006.
Farina, D., R. Merletti, and R. M. Enoka. The extraction of neural strategies from the surface EMG. J. Appl. Physiol. 96:1486–1495, 2004.
Gage, W. H., R. J. Sleik, M. A. Polych, N. C. McKenzie, and L. A. Brown. The allocation of attention during locomotion is altered by anxiety. Exp. Brain Res. 150:385–394, 2003.
Glascher, J., D. Tranel, L. K. Paul, D. Rudrauf, C. Rorden, A. Hornaday, T. Grabowski, H. Damasio, and R. Adolphs. Lesion mapping of cognitive abilities linked to intelligence. Neuron 61:681–691, 2009.
Grillner, S., P. Wallen, K. Saitoh, A. Kozlov, and B. Robertson. Neural bases of goal-directed locomotion in vertebrates—an overview. Brain Res. Rev. 57:2–12, 2008.
Grinsted, A., J. C. Moore, and S. Jevrejeva. Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Proc. Geophys. 11:561–566, 2004.
Grosse, P., M. J. Cassidy, and P. Brown. EEG-EMG, MEG-EMG and EMG–EMG frequency analysis: physiological principles and clinical applications. Clin. Neurophysiol. 113:1523–1531, 2002.
Halliday, D. M., B. A. Conway, S. F. Farmer, and J. R. Rosenberg. Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neurosci. Lett. 241:5–8, 1998.
Hansen, N. L., B. A. Conway, D. M. Halliday, S. Hansen, H. S. Pyndt, F. Biering-Sorensen, and J. B. Nielsen. Reduction of common synaptic drive to ankle dorsiflexor motoneurons during walking in patients with spinal cord lesion. J. Neurophysiol. 94:934–942, 2005.
Johnson, A. N., L. A. Wheaton, and M. Shinohara. Attenuation of corticomuscular coherence with additional motor or non-motor task. Clin. Neurophysiol. 122:356–363, 2011.
Kamen, G., and D. A. Gabriel. Essentials of Electromyography. Champaign, IL: Human Kinetics, 2010.
Kilner, J. M., S. N. Baker, S. Salenius, R. Hari, and R. N. Lemon. Human cortical muscle coherence is directly related to specific motor parameters. J. Neurosci. 20:8838–8845, 2000.
Kilner, J. M., S. N. Baker, S. Salenius, V. Jousmaki, R. Hari, and R. N. Lemon. Task-dependent modulation of 15–30 Hz coherence between rectified EMGs from human hand and forearm muscles. J. Physiol. 516(Pt 2):559–570, 1999.
Kristeva-Feige, R., C. Fritsch, J. Timmer, and C. H. Lucking. Effects of attention and precision of exerted force on beta range EEG-EMG synchronization during a maintained motor contraction task. Clin. Neurophysiol. 113:124–131, 2002.
Matsuyama, K., F. Mori, K. Nakajima, T. Drew, M. Aoki, and M. Shigemi. Locomotor Role of the Corticoreticular-Reticulospinal-Spinal Interneuronal System. Elsevier: Amsterdam, pp. 239–249, 2004.
McClelland, V. M., Z. Cvetkovic, and K. R. Mills. Rectification of the EMG is an unnecessary and inappropriate step in the calculation of corticomuscular coherence. J. Neurosci. Methods 205:190–201, 2012.
Murthy, V. N., and E. E. Fetz. Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc. Natl. Acad. Sci. USA 89:5670–5674, 1992.
Neto, O. P., H. S. Baweja, and E. A. Christou. Increased voluntary drive is associated with changes in common oscillations from 13 to 60 Hz of interference but not rectified electromyography. Muscle Nerve 42:348–354, 2010.
Neto, O. P., and E. A. Christou. Rectification of the EMG signal impairs the identification of oscillatory input to the muscle. J. Neurophysiol. 103:1093–1103, 2010.
Nielsen, J. B. How we walk: central control of muscle activity during human walking. Neuroscientist 9:195–204, 2003.
Nielsen, J. B., J. S. Brittain, D. M. Halliday, V. Marchand-Pauvert, D. Mazevet, and B. A. Conway. Reduction of common motoneuronal drive on the affected side during walking in hemiplegic stroke patients. Clin. Neurophysiol. 119:2813–2818, 2008.
Norton, J. A., and M. A. Gorassini. Changes in cortically related intermuscular coherence accompanying improvements in locomotor skills in incomplete spinal cord injury. J. Neurophysiol. 95:2580–2589, 2006.
Omlor, W., L. Patino, M. C. Hepp-Reymond, and R. Kristeva. Gamma-range corticomuscular coherence during dynamic force output. Neuroimage 34:1191–1198, 2007.
Perroto, A. O. Anatomical Guide for the Electromyographer (3rd ed.). Springfield, IL: Charles C. Thomas, 1994.
Petersen, N. T., J. E. Butler, V. Marchand-Pauvert, R. Fisher, A. Ledebt, H. S. Pyndt, N. L. Hansen, and J. B. Nielsen. Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking. J. Physiol. 537:651–656, 2001.
Petersen, T. H., M. Kliim-Due, S. F. Farmer, and J. B. Nielsen. Childhood development of common drive to a human leg muscle during ankle dorsiflexion and gait. J. Physiol. 588:4387–4400, 2010.
Petersen, T. H., M. Willerslev-Olsen, B. A. Conway, and J. B. Nielsen. The motor cortex drives the muscles during walking in human subjects. J. Physiol. 590(Pt 10):2443–2452, 2012.
Regnaux, J. P., D. David, O. Daniel, D. B. Smail, M. Combeaud, and B. Bussel. Evidence for cognitive processes involved in the control of steady state of walking in healthy subjects and after cerebral damage. Neurorehabil. Neural Repair 19:125–132, 2005.
Salenius, S., K. Portin, M. Kajola, R. Salmelin, and R. Hari. Cortical control of human motoneuron firing during isometric contraction. J. Neurophysiol. 77:3401–3405, 1997.
Schubert, M., A. Curt, G. Colombo, W. Berger, and V. Dietz. Voluntary control of human gait: conditioning of magnetically evoked motor responses in a precision stepping task. Exp. Brain Res. 126:583–588, 1999.
Schubert, M., A. Curt, L. Jensen, and V. Dietz. Corticospinal input in human gait: modulation of magnetically evoked motor responses. Exp. Brain Res. 115:234–246, 1997.
Seidler, R. D., J. A. Bernard, T. B. Burutolu, B. W. Fling, M. T. Gordon, J. T. Gwin, Y. Kwak, and D. B. Lipps. Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci. Biobehav. Rev. 34:721–733, 2010.
Suzuki, M., I. Miyai, T. Ono, and K. Kubota. Activities in the frontal cortex and gait performance are modulated by preparation. An fNIRS study. Neuroimage 39:600–607, 2008.
Torrence, C., and G. P. Compo. A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc. 79:61–78, 1998.
Varraine, E., M. Bonnard, and J. Pailhous. Intentional on-line adaptation of stride length in human walking. Exp. Brain Res. 130:248–257, 2000.
Acknowledgments
This work was supported by the US Department of Veterans Affairs Rehabilitation Research and Development Service (B7176W to DJC) and by the National Institute on Aging (P30-AG028740-04 to DJC and R01 AG-031769 to EAC).
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Associate Editor Catherine Disselhorst-Klug oversaw the review of this article.
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Clark, D.J., Kautz, S.A., Bauer, A.R. et al. Synchronous EMG Activity in the Piper Frequency Band Reveals the Corticospinal Demand of Walking Tasks. Ann Biomed Eng 41, 1778–1786 (2013). https://doi.org/10.1007/s10439-013-0832-4
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DOI: https://doi.org/10.1007/s10439-013-0832-4