Recruitment and rate coding organisation for soleus motor units across entire range of voluntary isometric plantar flexions

Unlike upper limb muscles, it remains undocumented as to how motor units in the soleus muscle are organised in terms of recruitment range and discharge rates with respect to their recruitment and de‐recruitment thresholds. The possible influence of neuromodulation, such as persistent inward currents (PICs) on lower limb motor unit recruitment and discharge rates has also yet to be reported. To address these issues, electromyographic (EMG) activities from the soleus muscle were recorded using selective branched‐wire intramuscular electrodes during ramp‐and‐hold contractions with intensities up to maximal voluntary contraction (MVC). The multiple single motor unit activities were then derived using a decomposition technique. The onset–offset hysteresis of motor unit discharge, i.e. a difference between recruitment and de‐recruitment thresholds, as well as PIC magnitude calculated by a paired motor unit analysis were used to examine the neuromodulatory effects on discharge behaviours, such as minimum firing rate, peak firing rate and degree of increase in firing rate. Forty‐two clearly identified motor units from five subjects revealed that soleus motor units are recruited progressively from rest to contraction strengths close to 95% of MVC, with low‐threshold motor units discharging action potentials slower at their recruitment and with a lower peak rate than later recruited high‐threshold units. This observation is in contrast to the ‘onion skin phenomenon’ often reported for the upper limb muscles. Based on positive correlations of the peak discharge rates, initial rates and recruitment order of the units with the magnitude of the onset–offset hysteresis and not PIC contribution, we conclude that discharge behaviours among motor units appear to be related to a variation in an intrinsic property other than PICs.

[1]  R. Powers,et al.  Estimation of the contribution of intrinsic currents to motoneuron firing based on paired motoneuron discharge records in the decerebrate cat. , 2008, Journal of neurophysiology.

[2]  D. Kosarov,et al.  Some features of different motor units in human biceps brachii , 1974, Pflügers Archiv.

[3]  R. Person,et al.  Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. , 1972, Electroencephalography and clinical neurophysiology.

[4]  Hans Hultborn,et al.  Key mechanisms for setting the input-output gain across the motoneuron pool. , 2004, Progress in brain research.

[5]  Roger M Enoka,et al.  Motor-unit activity differs with load type during a fatiguing contraction. , 2005, Journal of neurophysiology.

[6]  V. Dietz,et al.  Activity of single motor units from human forearm muscles during voluntary isometric contractions. , 1975, Journal of neurophysiology.

[7]  J. Feldman,et al.  Synaptic control of motoneuronal excitability. , 2000, Physiological reviews.

[8]  C. D. De Luca,et al.  Behaviour of human motor units in different muscles during linearly varying contractions , 1982, The Journal of physiology.

[9]  M. Gorassini,et al.  Persistent inward currents in motoneuron dendrites: Implications for motor output , 2005, Muscle & nerve.

[10]  H. Clamann,et al.  Elsevier/North-Holland Biomedical Press COMPARISON OF THE RECRUITMENT AND DISCHARGE PROPERTIES OF MOTOR UNITS IN H U M A N BRACHIAL BICEPS AND A D D U C T O R POLLICIS D U R I N G ISOMETRIC CONTRACTIONS , 2018 .

[11]  J. Duchateau,et al.  Mechanical properties and behaviour of motor units in the tibialis anterior during voluntary contractions. , 1997, Canadian journal of applied physiology = Revue canadienne de physiologie appliquee.

[12]  Jaynie F. Yang,et al.  Intrinsic activation of human motoneurons: possible contribution to motor unit excitation. , 2002, Journal of neurophysiology.

[13]  O. Kiehn,et al.  Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? , 1997, Journal of neurophysiology.

[14]  Kevin C. McGill,et al.  EMGLAB: An interactive EMG decomposition program , 2005, Journal of Neuroscience Methods.

[15]  G. A. Robinson,et al.  A stable, selective electrode for recording single motor-unit potentials in humans , 1988, Experimental Neurology.

[16]  D. Kernell The Limits of Firing Frequency in Cat Lumbosacral Motoneurones Possessing Different Time Course of Afterhyperpolarization , 1965 .

[17]  Andrew J Fuglevand,et al.  Evaluation of plateau‐potential‐mediated ‘warm up’ in human motor units , 2006, The Journal of physiology.

[18]  H Hultborn,et al.  Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. , 1998, Journal of neurophysiology.

[19]  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.

[20]  C. Heckman,et al.  Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. , 1998, Journal of neurophysiology.

[21]  N. Trayanova,et al.  Selective recording of motor unit potentials. , 1986, Electromyography and clinical neurophysiology.

[22]  O. Kiehn,et al.  Bistability of alpha‐motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5‐hydroxytryptophan. , 1988, The Journal of physiology.

[23]  H. Freund Motor unit and muscle activity in voluntary motor control. , 1983, Physiological reviews.

[24]  Kevin C McGill,et al.  Electrophysiological evidence of adult human skeletal muscle fibres with multiple endplates and polyneuronal innervation , 2002, The Journal of physiology.

[25]  B Bigland-Ritchie,et al.  Motor-unit discharge rates in maximal voluntary contractions of three human muscles. , 1983, Journal of neurophysiology.

[26]  M D Binder,et al.  Computer simulations of motoneuron firing rate modulation. , 1993, Journal of neurophysiology.

[27]  A. Thorstensson,et al.  Influence of gastrocnemius muscle length on triceps surae torque development and electromyographic activity in man , 1995, Experimental Brain Research.

[28]  島津 浩,et al.  Functional differentiation of human skeletal muscle : corticalization and spinalization of movement , 1964 .

[29]  J. Hannerz,et al.  Contraction time and voluntary discharge properties of individual short toe extensor motor units in man. , 1979, The Journal of physiology.

[30]  C J De Luca,et al.  Rank‐ordered regulation of motor units , 1996, Muscle & nerve.

[31]  A. Monster,et al.  Isometric force production by motor units of extensor digitorum communis muscle in man. , 1977, Journal of neurophysiology.

[32]  R. Stein,et al.  Motor-unit recruitment in human first dorsal interosseous muscle for static contractions in three different directions. , 1986, Journal of neurophysiology.

[33]  C. Heckman,et al.  Persistent Inward Currents in Spinal Motoneurons and Their Influence on Human Motoneuron Firing Patterns , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[34]  J. Vedel,et al.  Comparison of fluctuations of motor unit recruitment and de-recruitment thresholds in man , 2004, Experimental Brain Research.

[35]  B. M. ter Haar Romeny,et al.  Behaviour of motor units of human arm muscles: differences between slow isometric contraction and relaxation. , 1985, The Journal of physiology.

[36]  C. Heckman,et al.  Adjustable Amplification of Synaptic Input in the Dendrites of Spinal Motoneurons In Vivo , 2000, The Journal of Neuroscience.