Skip to main content
Log in

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

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. 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.

    Article  PubMed  CAS  Google Scholar 

  2. 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.

    Article  PubMed  CAS  Google Scholar 

  3. 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.

    Article  PubMed  Google Scholar 

  4. 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.

    Article  PubMed  Google Scholar 

  5. 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.

    Article  PubMed  Google Scholar 

  6. 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.

    Article  PubMed  Google Scholar 

  7. 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.

    Article  PubMed  Google Scholar 

  8. Brown, P. Cortical drives to human muscle: the Piper and related rhythms. Prog. Neurobiol. 60:97–108, 2000.

    Article  PubMed  CAS  Google Scholar 

  9. Brown, P., S. Salenius, J. C. Rothwell, and R. Hari. Cortical correlate of the Piper rhythm in humans. J. Neurophysiol. 80:2911–2917, 1998.

    PubMed  CAS  Google Scholar 

  10. 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.

    Article  Google Scholar 

  11. Christou, E. A., and O. P. Neto. Reply to Boonstra: the nature of periodic input to the muscle. J. Neurophysiol. 104:577, 2010.

    Article  Google Scholar 

  12. 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.

    PubMed  CAS  Google Scholar 

  13. de Leva, P. Adjustments to Zatsiorsky-Seluyanov’s segment inertia parameters. J. Biomech. 29:1223–1230, 1996.

    Article  PubMed  Google Scholar 

  14. De Luca, C. J. The use of surface electromyography in biomechanics. J. Appl. Biomech. 13:135–163, 1997.

    Google Scholar 

  15. Drew, T. Motor cortical cell discharge during voluntary gait modification. Brain Res. 457:181–187, 1988.

    Article  PubMed  CAS  Google Scholar 

  16. Farina, D. Interpretation of the surface electromyogram in dynamic contractions. Exerc. Sport Sci. Rev. 34:121–127, 2006.

    Article  PubMed  Google Scholar 

  17. Farina, D., R. Merletti, and R. M. Enoka. The extraction of neural strategies from the surface EMG. J. Appl. Physiol. 96:1486–1495, 2004.

    Article  PubMed  Google Scholar 

  18. 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.

    PubMed  Google Scholar 

  19. 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.

    Article  PubMed  CAS  Google Scholar 

  20. 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.

    Article  PubMed  Google Scholar 

  21. 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.

    Article  Google Scholar 

  22. 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.

    Article  PubMed  CAS  Google Scholar 

  23. 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.

    Article  PubMed  CAS  Google Scholar 

  24. 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.

    Article  PubMed  CAS  Google Scholar 

  25. 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.

    Article  PubMed  Google Scholar 

  26. Kamen, G., and D. A. Gabriel. Essentials of Electromyography. Champaign, IL: Human Kinetics, 2010.

    Google Scholar 

  27. 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.

    PubMed  CAS  Google Scholar 

  28. 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.

    Article  PubMed  CAS  Google Scholar 

  29. 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.

    Article  PubMed  Google Scholar 

  30. 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.

  31. 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.

    Article  PubMed  Google Scholar 

  32. 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.

    Article  PubMed  CAS  Google Scholar 

  33. 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.

    Article  PubMed  Google Scholar 

  34. 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.

    Article  PubMed  Google Scholar 

  35. Nielsen, J. B. How we walk: central control of muscle activity during human walking. Neuroscientist 9:195–204, 2003.

    Article  PubMed  Google Scholar 

  36. 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.

    Article  PubMed  CAS  Google Scholar 

  37. 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.

    Article  PubMed  Google Scholar 

  38. Omlor, W., L. Patino, M. C. Hepp-Reymond, and R. Kristeva. Gamma-range corticomuscular coherence during dynamic force output. Neuroimage 34:1191–1198, 2007.

    Article  PubMed  Google Scholar 

  39. Perroto, A. O. Anatomical Guide for the Electromyographer (3rd ed.). Springfield, IL: Charles C. Thomas, 1994.

    Google Scholar 

  40. 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.

    Article  PubMed  CAS  Google Scholar 

  41. 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.

    Article  PubMed  CAS  Google Scholar 

  42. 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.

    PubMed  CAS  Google Scholar 

  43. 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.

    Article  PubMed  CAS  Google Scholar 

  44. 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.

    PubMed  CAS  Google Scholar 

  45. 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.

    Article  PubMed  CAS  Google Scholar 

  46. 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.

    Article  PubMed  CAS  Google Scholar 

  47. 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.

    Article  PubMed  CAS  Google Scholar 

  48. 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.

    Article  PubMed  Google Scholar 

  49. Torrence, C., and G. P. Compo. A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc. 79:61–78, 1998.

    Article  Google Scholar 

  50. Varraine, E., M. Bonnard, and J. Pailhous. Intentional on-line adaptation of stride length in human walking. Exp. Brain Res. 130:248–257, 2000.

    Article  PubMed  CAS  Google Scholar 

Download references

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).

Conflicts of Interest

There are no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David J. Clark.

Additional information

Associate Editor Catherine Disselhorst-Klug oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-013-0832-4

Keywords

Navigation