Motor unit synchronization during fatigue: described with a novel sEMG method based on large motor unit samples.

The amount of documented increase in motor unit (MU) synchronization with fatigue and its possible relation with force tremor varies largely, possibly due to inhomogeneous muscle activation and methodological discrepancies and limitations. The aim of this study was to apply a novel surface electromyographical (EMG) descriptor for MU synchronization based on large MU populations to examine changes in MU synchronization with fatigue at different sites of a muscle and its relation to tremor. Twenty-four subjects performed an isometric elbow flexion at 25% of maximal voluntary contraction until exhaustion. Monopolar EMG signals were recorded using a grid of 130 electrodes above the biceps brachii. Changes in MU synchronization were estimated based on the sub-band skewness of EMG signals and tremor by the coefficient of variation in force. The synchronization descriptor was dependent on recording site and increased with fatigue together with tremor. There was a general association between these two parameters, but not between their fluctuations. These results are in agreement with other surface EMG studies and indicate that the novel descriptor can be used to attain information of synchronization between large MU populations during fatigue that cannot be retrieved with intra-muscular EMG.

[1]  V. Dietz,et al.  Neuronal mechanisms underlying physiological tremor. , 1978, Journal of neurophysiology.

[2]  T. Sadoyama,et al.  Topographical map of innervation zones within single motor units measured with a grid surface electrode , 1988, IEEE Transactions on Biomedical Engineering.

[3]  E. Jankowska,et al.  Projections of pyramidal tract cells to alpha‐motoneurones innervating hind‐limb muscles in the monkey. , 1975, The Journal of physiology.

[4]  J. Stephens,et al.  Effect of task on the degree of synchronization of intrinsic hand muscle motor units in man. , 1991, Journal of neurophysiology.

[5]  T. Hortobágyi,et al.  Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. , 2003, Journal of neurophysiology.

[6]  J. R. Rosenberg,et al.  Load-independent contributions from motor-unit synchronization to human physiological tremor. , 1999, Journal of neurophysiology.

[7]  K Sakamoto,et al.  Contribution of motor unit activity enhanced by acute fatigue to physiological tremor of finger. , 1999, Electromyography and clinical neurophysiology.

[8]  R. Enoka,et al.  Coactivation of the antagonist muscle does not covary with steadiness in old adults. , 2000, Journal of applied physiology.

[9]  A Forster,et al.  Changes in muscle fiber conduction velocity, mean power frequency, and mean EMG voltage during prolonged submaximal contractions , 1989, Muscle & nerve.

[10]  K. Roeleveld,et al.  Inhomogeneities in muscle activation reveal motor unit recruitment. , 2005, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[11]  F BUCHTHAL,et al.  Synchronous activity in normal and atrophic muscle. , 1950, Electroencephalography and clinical neurophysiology.

[12]  E Henneman,et al.  Terminals of single Ia fibers: location, density, and distribution within a pool of 300 homonymous motoneurons. , 1971, Journal of neurophysiology.

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

[14]  R. Elble,et al.  Motor-unit activity responsible for 8- to 12-Hz component of human physiological finger tremor. , 1976, Journal of neurophysiology.

[15]  A. Fuglevand,et al.  Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle. , 2004, Journal of neurophysiology.

[16]  O. A. Nikitin,et al.  Neither high-pass filtering nor mathematical differentiation of the EMG signals can considerably reduce cross-talk. , 2002, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[17]  Roger M Enoka,et al.  Multiple features of motor-unit activity influence force fluctuations during isometric contractions. , 2003, Journal of neurophysiology.

[18]  O. Lippold.  Oscillation in the stretch reflex arc and the origin of the rhythmical, 8–12 c/s component of physiological tremor , 1970, The Journal of physiology.

[19]  John G Semmler,et al.  Motor Unit Synchronization and Neuromuscular Performance , 2002, Exercise and sport sciences reviews.

[20]  R. Enoka,et al.  Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. , 2000, Journal of neurophysiology.

[21]  D. Farina,et al.  Nonlinear surface EMG analysis to detect changes of motor unit conduction velocity and synchronization. , 2002, Journal of applied physiology.

[22]  J. Semmler,et al.  Motor unit discharge and force tremor in skill- and strength-trained individuals , 1998, Experimental Brain Research.

[23]  D. Stegeman,et al.  Influence of motoneuron firing synchronization on SEMG characteristics in dependence of electrode position. , 2001, Journal of applied physiology.

[24]  Roger M Enoka,et al.  Changes in muscle activation can prolong the endurance time of a submaximal isometric contraction in humans. , 2003, Journal of applied physiology.

[25]  Karin Roeleveld,et al.  Spatial distribution of active muscle fibre characteristics in the upper trapezius muscle and its dependency on contraction level and duration. , 2008, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[26]  P. Matthews,et al.  Comparison of electromyogram spectra with force spectra during human elbow tremor. , 1980, The Journal of physiology.

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

[28]  J. Vedel,et al.  Motor unit synchronous firing as revealed by determinism of surface myoelectric signal , 2006, Journal of Neuroscience Methods.

[29]  Catherine Disselhorst-Klug,et al.  Simulation analysis of the ability of different types of multi-electrodes to increase selectivity of detection and to reduce cross-talk. , 2003, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[30]  J. Redfearn,et al.  An analysis of the frequencies of finger tremor in healthy subjects , 1956, The Journal of physiology.

[31]  F Bruyninckx,et al.  Motor unit synchronization in physiologic, enhanced physiologic, and voluntary tremor in man , 1988, Annals of neurology.

[32]  C. Gielen,et al.  Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different tasks , 1984, Experimental Neurology.

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

[34]  G Rau,et al.  Non-invasive detection of the single motor unit action potential by averaging the spatial potential distribution triggered on a spatially filtered motor unit action potential. , 1999, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[35]  G. A. Robinson,et al.  Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. , 1994, Journal of applied physiology.

[36]  J A Stephens,et al.  Correlation between the discharges of motor units recorded from the same and from different finger muscles in man. , 1991, The Journal of physiology.

[37]  K Roeleveld,et al.  Motor unit synchronization during fatigue: a novel quantification method. , 2009, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[38]  Tadashi Masuda,et al.  Distribution of innervation zones in the human biceps brachii. , 1991, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[39]  Electromyographic responses of the human triceps surae and force tremor during sustained submaximal isometric plantar flexion. , 1994, Acta physiologica Scandinavica.

[40]  S. Mori,et al.  Discharge patterns of soleus motor units with associated changes in force exerted by foot during quiet stance in man. , 1973, Journal of neurophysiology.

[41]  A. J. Lloyd,et al.  Surface electromyography during sustained isometric contractions. , 1971, Journal of applied physiology.

[42]  T. Sears,et al.  Short‐term synchronization of intercostal motoneurone activity. , 1976, The Journal of physiology.

[43]  Marc H Schieber,et al.  Short-term synchronization between motor units in different functional subdivisions of the human flexor digitorum profundus muscle. , 2004, Journal of neurophysiology.

[44]  O. Lippold,et al.  Motor unit activity in the voluntary contraction of human muscle , 1954, The Journal of physiology.

[45]  R. Enoka,et al.  Mechanisms that contribute to differences in motor performance between young and old adults. , 2003, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[46]  D. F. Stegeman,et al.  Selective spatial information from surface EMG after temporal filtering: the application to interference EMG using cross-covariance analysis , 2003, Clinical Neurophysiology.

[47]  C. Marsden,et al.  Frequency peaks of tremor, muscle vibration and electromyographic activity at 10 Hz, 20 Hz and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing , 1997, Experimental Brain Research.

[48]  R. Stein,et al.  Synchronization of human motor units: possible roles of exercise and supraspinal reflexes. , 1975, Electroencephalography and clinical neurophysiology.

[49]  V. Dietz,et al.  Correlation between the dischanges of two simultaneously recorded motor units and physiological tremor. , 1976, Electroencephalography and clinical neurophysiology.

[50]  J. Stefan Karlsson,et al.  On-line signal quality estimation of multichannel surface electromyograms , 2005, Medical and Biological Engineering and Computing.

[51]  Michael A Nordstrom,et al.  A comparison of cross-correlation and surface EMG techniques used to quantify motor unit synchronization in humans , 1999, Journal of Neuroscience Methods.

[52]  R. Elble.  Central mechanisms of tremor. , 1996, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.