Background Neuroplasticity drives recovery of walking after a lesion of the descending tract. Intramuscular coherence analysis provides a way to quantify corticomotor drive during a functional task, like walking and changes in coherence serve as a marker for neuroplasticity. Although intramuscular coherence analysis is already applied and rapidly growing in interest, the reproducibility of variables derived from coherence is largely unknown. The purpose of this study was to determine the test-retest reliability and agreement of intramuscular coherence variables obtained during walking in healthy subjects. Methodology/Principal Findings Ten healthy participants walked on a treadmill at a slow and normal speed in three sessions. Area of coherence and peak coherence were derived from the intramuscular coherence spectra calculated using rectified and non-rectified M. tibialis anterior Electromyography (EMG). Reliability, defined as the ability of a measurement to differentiate between subjects and established by the intra-class correlation coefficient, was on the limit of good for area of coherence and peak coherence when derived from rectified EMG during slow walking. Yet, the agreement, defined as the degree to which repeated measures are identical, was low as the measurement error was relatively large. The smallest change to exceed the measurement error between two repeated measures was 66% of the average value. For normal walking and/or other EMG-processing settings, not rectifying the EMG and/or high-pass filtering with a high cutoff frequency (100 Hz) the reliability was only moderate to poor and the agreement was considerably lower. Conclusions/significance Only for specific conditions and EMG-processing settings, the derived coherence variables can be considered to be reliable measures. However, large changes (>66%) are needed to indicate a real difference. So, although intramuscular coherence is an easy to use and a sufficiently reliable tool to quantify intervention-induced neuroplasticity, the large effects needed to reveal a real change limit its practical use.
References
[1]
Cramer SC, Sur M, Dobkin BH, O'Brien C, Sanger TD, et al. (2011) Harnessing neuroplasticity for clinical applications. Brain 134: 1591–1609 doi:10.1093/brain/awr039.
[2]
Nielsen J (2002) Motoneuronal drive during human walking. Brain Res Rev 40: 192–201. doi: 10.1016/s0165-0173(02)00201-1
[3]
Hansen NL, Hansen S, Christensen LO, Petersen NT, Nielsen JB (2001) Synchronization of lower limb motor unit activity during walking in human subjects. J Neurophysiol 86: 1266–1276.
[4]
Grosse P, Guerrini R, Parmeggiani L, Bonanni P, Pogosyan A, et al. (2003) Abnormal corticomuscular and intermuscular coupling in high-frequency rhythmic myoclonus. Brain 126: 326–342. doi: 10.1093/brain/awg043
[5]
Halliday DM, Conway BA, Christensen LOD, Hansen NL, Petersen NP, et al. (2003) Functional coupling of motor units is modulated during walking in human subjects. Journal of Neurophysiology 89: 960–968 doi:10.1152/jn.00844.2002.
[6]
Grosse P, Cassidy M, Brown P (2002) EEG-EMG, MEG-EMG and EMG-EMG frequency analysis: physiological principles and clinical applications. Clin Neurophysiol 113: 1523–1531. doi: 10.1016/s1388-2457(02)00223-7
[7]
Petersen TH, Kliim-Due M, Farmer SF, Nielsen JB (2010) Childhood development of common drive to a human leg muscle during ankle dorsiflexion and gait. Journal of Physiology 588: 4387–4400 doi:10.1113/jphysiol.2010.195735.
[8]
Brown P, Farmer SF, Halliday DM, Marsden J, Rosenberg JR (1999) Coherent cortical and muscle discharge in cortical myoclonus. Brain 122 Pt 3461–472. doi: 10.1093/brain/122.3.461
[9]
Norton JA, Wood DE, Day BL (2004) Is the spinal cord the generator of 16-Hz orthostatic tremor? Neurology 62: 632–634. doi: 10.1212/wnl.62.4.632
[10]
Norton JA, Wood DE, Marsden JF, Day BL (2003) Spinally generated electromyographic oscillations and spasms in a low-thoracic complete paraplegic. Mov Disord 18: 101–106 doi:10.1002/mds.10298.
[11]
Barthélemy D, Willerslev-Olsen M, Lundell H, Conway BA, Knudsen H, et al. (2010) Impaired transmission in the corticospinal tract and gait disability in spinal cord injured persons. J Neurophysiol 104: 1167–1176 doi:10.1152/jn.00382.2010.
[12]
Hansen NL, Conway BA, Halliday DM, Hansen S, Pyndt HS, et al. (2005) Reduction of common synaptic drive to ankle dorsiflexor motoneurons during walking in patients with spinal cord lesion. J Neurophysiol 94: 934–942 doi:10.1152/jn.00082.2005.
[13]
Norton JA (2008) Higher neural control is required for functional walking. Clin Neurophysiol 119: 2675–2676. doi: 10.1016/j.clinph.2008.08.014
[14]
Nielsen JB, Brittain J-S, Halliday DM, Marchand-Pauvert V, Mazevet D, et al. (2008) Reduction of common motoneuronal drive on the affected side during walking in hemiplegic stroke patients. Clin Neurophysiol 119: 2813–2818 doi:10.1016/j.clinph.2008.07.283.
[15]
Norton JA, Gorassini MA (2006) Changes in cortically related intermuscular coherence accompanying improvements in locomotor skills in incomplete spinal cord injury. J Neurophysiol 95: 2580–2589 doi:10.1152/jn.01289.2005.
[16]
Rogers LM, Madhavan S, Roth H, Stinear JW (2011) Transforming neurorehabilitation of walking following stroke: The promise of non-invasive brain stimulation - a review. Restor Neurol Neurosci 29: 507–516 doi:10.3233/RNN-2011-0625.
[17]
Power HA, Norton JA, Porter CL, Doyle Z, Hui I, et al. (2006) Transcranial direct current stimulation of the primary motor cortex affects cortical drive to human musculature as assessed by intermuscular coherence. J Physiol 577: 795–803 doi:10.1113/jphysiol.2006.116939.
[18]
Perez MA, Lundbye-Jensen J, Nielsen JB (2006) Changes in corticospinal drive to spinal motoneurones following visuo-motor skill learning in humans. The Journal of Physiology 573: 843–855 doi:10.1113/jphysiol.2006.105361.
[19]
Farina D, Negro F, Jiang N (2013) Identification of common synaptic inputs to motor neurons from the rectified electromyogram. J Physiol 591: 2403–2418. doi: 10.1113/jphysiol.2012.246082
[20]
McClelland VM, Cvetkovic Z, Mills KR (2012) Rectification of the EMG is an unnecessary and inappropriate step in the calculation of Corticomuscular coherence. J Neurosci Methods 205: 190–201. doi: 10.1016/j.jneumeth.2011.11.001
[21]
Stegeman DF, van de Ven WJM, van Elswijk GA, Oostenveld R, Kleine BU (2010) The alpha-motoneuron pool as transmitter of rhythmicities in cortical motor drive. Clin Neurophysiol 121: 1633–1642 doi:10.1016/j.clinph.2010.03.052.
[22]
Halliday DM, Farmer SF (2010) On the need for rectification of surface EMG. J Neurophysiol 103: 3547–authorreply3548–9 doi:10.1152/jn.00222.2010.
[23]
Neto OP, Christou EA (2010) Rectification of the EMG signal impairs the identification of oscillatory input to the muscle. J Neurophysiol 103: 1093–1103 doi:10.1152/jn.00792.2009.
[24]
Yao B, Salenius S, Yue GH, Brown RW, Liu JZ (2007) Effects of surface EMG rectification on power and coherence analyses: An EEG and MEG study. J Neurosci Methods 159: 215–223 doi:10.1016/j.jneumeth.2006.07.008.
[25]
Myers LJ, Lowery M, O'malley M, Vaughan CL, Heneghan C, et al. (2003) Rectification and non-linear pre-processing of EMG signals for cortico-muscular analysis. J Neurosci Methods 124: 157–165. doi: 10.1016/s0165-0270(03)00004-9
[26]
Boonstra TW, Breakspear M (2012) Neural mechanisms of intermuscular coherence: implications for the rectification of surface electromyography. J Neurophysiol 107: 796–807 doi:10.1152/jn.00066.2011.
[27]
Ward NJ, Farmer SF, Berthouze L, Halliday DM (2013) Rectification of EMG in low force contractions improves detection of motor unit coherence in the beta-frequency band. J Neurophysiol 110: 1744–1750 doi:10.1152/jn.00296.2013.
[28]
Potvin JR, Brown SHM (2004) Less is more: high pass filtering, to remove up to 99% of the surface EMG signal power, improves EMG-based biceps brachii muscle force estimates. J Electromyogr Kinesiol 14: 389–399 doi:10.1016/j.jelekin.2003.10.005.
[29]
Staudenmann D, Potvin JR, Kingma I, Stegeman DF, van Die？n JH (2007) Effects of EMG processing on biomechanical models of muscle joint systems: sensitivity of trunk muscle moments, spinal forces, and stability. J Biomech 40: 900–909 doi:10.1016/j.jbiomech.2006.03.021.
[30]
de Vet HCW, Terwee CB, Knol DL, Bouter LM (2006) When to use agreement versus reliability measures. J Clin Epidemiol 59: 1033–1039 doi:10.1016/j.jclinepi.2005.10.015.
[31]
Kottner J, Audigé L, Brorson S, Donner A, Gajewski BJ, et al. (2011) Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. J Clin Epidemiol 64: 96–106 doi:10.1016/j.jclinepi.2010.03.002.
[32]
De Ruiter CJ, De Korte A, Schreven S, de Haan A (2010) Leg dominancy in relation to fast isometric torque production and squat jump height. Eur J Appl Physiol 108: 247–255 doi:10.1007/s00421-009-1209-0.
[33]
Nitsche M, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57: 1899–1901. doi: 10.1212/wnl.57.10.1899
[34]
Roy RR, Garfinkel A, Ounjian M, Payne J, Hirahara A, et al. (1995) Three-dimensional structure of cat tibialis anterior motor units. Muscle Nerve 18: 1187–1195 doi:10.1002/mus.880181015.
[35]
Otter den A, Geurts A, Mulder T, Duysens J (2004) Speed related changes in muscle activity from normal to very slow walking speeds. Gait Posture 19: 270–278. doi: 10.1016/s0966-6362(03)00071-7
[36]
Priestley MB (1983) Spectral analysis and time series. Academic Press. 1 pp.
[37]
Oostenveld R, Fries P, Maris E, Schoffelen J-M (2011) FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data. Computational Intelligence and Neuroscience 2011: 156869 doi:10.1155/2011/156869.
[38]
Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM (1989) The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53: 1–31. doi: 10.1016/0079-6107(89)90004-7
[39]
Portney LG, Watkins MP (2009) Foundations of clinical research. Prentice Hall. 1 pp.
[40]
Beckerman H, Roebroeck ME, Lankhorst GJ, Becher JG, Bezemer PD, et al. (2001) Smallest real difference, a link between reproducibility and responsiveness. Qual Life Res 10: 571–578. doi: 10.1023/a:1013138911638
[41]
Wagner JM, Rhodes JA, Patten C (2008) Reproducibility and minimal detectable change of three-dimensional kinematic analysis of reaching tasks in people with hemiparesis after stroke. Phys Ther 88: 652–663 doi:10.2522/ptj.20070255.
[42]
Pohja M, Salenius S, Hari R (2005) Reproducibility of cortex-muscle coherence. NeuroImage 26: 764–770 doi:10.1016/j.neuroimage.2005.02.031.
[43]
Hausdorff JM (2007) Gait dynamics, fractals and falls: Finding meaning in the stride-to-stride fluctuations of human walking. Hum Mov Sci.
[44]
Hausdorff JM, Peng CK, Ladin Z, Wei JY, Goldberger AL (1995) Is walking a random walk? Evidence for long-range correlations in stride interval of human gait. J Appl Physiol 78: 349–358.
[45]
Farmer SF, Bremner FD, Halliday DM, Rosenberg JR, Stephens JA (1993) The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J Physiol 470: 127–155.
[46]
Negro F, Farina D (2011) Linear transmission of cortical oscillations to the neural drive to muscles is mediated by common projections to populations of motoneurons in humans. J Physiol 589: 629–637 doi:10.1113/jphysiol.2010.202473.
[47]
Petersen TH, Willerslev-Olsen M, Conway BA, Nielsen JB (2012) The motor cortex drives the muscles during walking in human subjects. J Physiol 590: 2443–2452 doi:10.1113/jphysiol.2012.227397.
[48]
Gwin JT, Ferris DP (2012) Beta- and gamma-range human lower limb corticomuscular coherence. Front Hum Neurosci 6 . doi:10.3389/fnhum.2012.00258.
