Fatigue related changes in electromyographic coherence between synergistic hand muscles

The aim of this study was to examine coherence between surface electromyographic (EMG) signals from two index finger flexor muscles, the first dorsal interosseous (FDI) and flexor digitorum superficialis (FDS), during and immediately following sustained, fatiguing isometric contraction. Coherence was observed between the FDI and FDS EMG signals in the tremor (8–12 Hz), beta (15–35 Hz) and gamma (35–60 Hz) bands in all subjects. A significant increase in EMG–EMG coherence in the beta and gamma frequency bands was observed immediately following the fatiguing contraction. No significant difference was observed in the tremor band coherence before and after fatigue. Coherence was observed between EMG and force in the tremor band during both the pre- and post-fatigue contractions and a significant increase in the FDI EMG-force coherence post-fatigue was observed. It is suggested that the increase in beta and gamma band coherence with fatigue may be due to increased levels of corticomotoneuronal drive to both muscles. Alternatively, the increased EMG–EMG coherence may reflect an increased contribution of peripheral afferents to coupling across the muscle with fatigue. Although the functional significance is not clear, the increase in coherence may help to overcome reduced motoneuron excitability with fatigue, to bind together different sensorimotor elements or to coordinate force generation across muscles in a more synergistic manner as the force generating capacity of the muscle is decreased.

[1]  J A Stephens,et al.  Variation in the degree of synchronization exhibited by motor units lying in different finger muscles in man. , 1991, The Journal of physiology.

[2]  C. Marsden,et al.  Physiological and pathological tremors and rhythmic central motor control. , 2000, Brain : a journal of neurology.

[3]  C. Krarup,et al.  Failure of activation of spinal motoneurones after muscle fatigue in healthy subjects studied by transcranial magnetic stimulation , 2003, The Journal of physiology.

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

[5]  P Ashby,et al.  Corticospinal projections to upper limb motoneurones in humans. , 1992, The Journal of physiology.

[6]  K. Terry,et al.  How computational technique and spike train properties affect coherence detection , 2008, Journal of Neuroscience Methods.

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

[8]  Zeynep Erim,et al.  Common drive of motor units in regulation of muscle force , 1994, Trends in Neurosciences.

[9]  Eberhard E. Fetz,et al.  Effects of Input Synchrony on the Firing Rate of a Three-Conductance Cortical Neuron Model , 1994, Neural Computation.

[10]  J. Bendat,et al.  Random Data: Analysis and Measurement Procedures , 1971 .

[11]  B Bigland-Ritchie,et al.  Fatigue of submaximal static contractions. , 1986, Acta physiologica Scandinavica. Supplementum.

[12]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[13]  T S Miles,et al.  Synchronization of motor units in human masseter during a prolonged isometric contraction. , 1990, The Journal of physiology.

[14]  T. Kuiken,et al.  A simulation study to examine the use of cross-correlation as an estimate of surface EMG cross talk. , 2003, Journal of applied physiology.

[15]  P. Rossini,et al.  Cortical short-term fatigue effects assessed via rhythmic brain–muscle coherence , 2006, Experimental Brain Research.

[16]  P. Welch.  The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[17]  G. Yue,et al.  Weakening of functional corticomuscular coupling during muscle fatigue , 2009, Brain Research.

[18]  Michael A. Nordstrom,et al.  Influence of handedness on motor unit discharge properties and force tremor , 2004, Experimental Brain Research.

[19]  J. Lundbye-Jensen,et al.  Changes in corticospinal drive to spinal motoneurones following visuo‐motor skill learning in humans , 2006, The Journal of physiology.

[20]  Madeleine M. Lowery,et al.  A Simulation Study to Examine the Effect of Common Motoneuron Inputs on Correlated Patterns of Motor Unit Discharge , 2005, Journal of Computational Neuroscience.

[21]  W. Z. Rymer,et al.  Evidence of shared, direct input to motoneurons supplying synergist muscles in humans , 1989, Neuroscience Letters.

[22]  C. G. Phillips,et al.  THE PYRAMIDAL PROJECTION TO MOTONEURONES OF SOME MUSCLE GROUPS OF THE BABOON'S FORELIMB. , 1964, Progress in brain research.

[23]  François G. Meyer,et al.  Motor-unit coherence and its relation with synchrony are influenced by training. , 2004, Journal of neurophysiology.

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

[25]  Madeleine M. Lowery,et al.  Coherence between motor unit discharges in response to shared neural inputs , 2007, Journal of Neuroscience Methods.

[26]  S. L. Richter,et al.  Guided waves in bounded media with random gross inhomogeneities , 1967 .

[27]  D. Halliday,et al.  The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. , 1993, The Journal of physiology.

[28]  Zeynep Erim,et al.  Journal of Neuroengineering and Rehabilitation Open Access Time and Frequency Domain Methods for Quantifying Common Modulation of Motor Unit Firing Patterns , 2004 .

[29]  Knaflitz,et al.  Myoelectric manifestations of fatigue in voluntary and electrically elicited contractions. , 1990, Journal of applied physiology.

[30]  Shi Zhou,et al.  Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle , 2002, The Journal of physiology.

[31]  K Roeleveld,et al.  Motor unit synchronization during fatigue: described with a novel sEMG method based on large motor unit samples. , 2009, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[32]  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.

[33]  Annie Schmied,et al.  Selective enhancement of motoneurone short-term synchrony during an attention-demanding task , 2000, Experimental Brain Research.

[34]  C. Moritz,et al.  Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. , 2005, Journal of neurophysiology.

[35]  M. Hallett,et al.  Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism , 1999, Clinical Neurophysiology.

[36]  P. Ellaway,et al.  Motor unit discharge characteristics and short term synchrony in paraplegic humans. , 1990, Journal of neurology, neurosurgery, and psychiatry.

[37]  Carlo J De Luca,et al.  Common drive in motor units of a synergistic muscle pair. , 2002, Journal of neurophysiology.

[38]  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.

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

[40]  A Schmied,et al.  Human spinal lateralization assessed from motoneurone synchronization: dependence on handedness and motor unit type. , 1994, The Journal of physiology.

[41]  Tamara J. Dartnall,et al.  Motor unit synchronization is increased in biceps brachii after exercise-induced damage to elbow flexor muscles. , 2008, Journal of neurophysiology.

[42]  Alexander Adam,et al.  Motor unit control and force fluctuation during fatigue. , 2009, Journal of applied physiology.

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

[44]  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.

[45]  R M Enoka,et al.  Motor-unit synchronization is not responsible for larger motor-unit forces in old adults. , 2000, Journal of neurophysiology.

[46]  C J De Luca,et al.  Synchronization of motor-unit firings in several human muscles. , 1993, Journal of neurophysiology.

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

[48]  D. Halliday,et al.  Changes in EMG coherence between long and short thumb abductor muscles during human development , 2007, The Journal of physiology.