Motor unit recruitment in human biceps brachii during sustained voluntary contractions

The purpose of the study was to examine the influence of the difference between the recruitment threshold of a motor unit and the target force of the sustained contraction on the discharge of the motor unit at recruitment. The discharge characteristics of 53 motor units in biceps brachii were recorded after being recruited during a sustained contraction. Some motor units (n= 22) discharged action potentials tonically after being recruited, whereas others (n= 31) discharged intermittent trains of action potentials. The two groups of motor units were distinguished by the difference between the recruitment threshold of the motor unit and the target force for the sustained contraction: tonic, 5.9 ± 2.5%; intermittent, 10.7 ± 2.9%. Discharge rate for the tonic units decreased progressively (13.9 ± 2.7 to 11.7 ± 2.6 pulses s−1; P= 0.04) during the 99 ± 111 s contraction. Train rate, train duration and average discharge rate for the intermittent motor units did not change across 211 ± 153 s of intermittent discharge. The initial discharge rate at recruitment during the sustained contraction was lower for the intermittent motor units (11.0 ± 3.3 pulses s−1) than the tonic motor units (13.7 ± 3.3 pulses s−1; P= 0.005), and the coefficient of variation for interspike interval was higher for the intermittent motor units (34.6 ± 12.3%) than the tonic motor units (21.2 ± 9.4%) at recruitment (P= 0.001) and remained elevated for discharge duration (34.6 ± 9.2%versus 19.1 ± 11.7%, P < 0.001). In an additional experiment, 12 motor units were recorded at two different target forces below recruitment threshold (5.7 ± 1.9% and 10.5 ± 2.4%). Each motor unit exhibited the two discharge patterns (tonic and intermittent) as observed for the 53 motor units. The results suggest that newly recruited motor units with recruitment thresholds closer to the target force experienced less synaptic noise at the time of recruitment that resulted in them discharging action potentials at more regular and greater rates than motor units with recruitment thresholds further from the target force.

[1]  C. Stevens,et al.  Synaptic noise and other sources of randomness in motoneuron interspike intervals. , 1968, Journal of neurophysiology.

[2]  J. Hannerz,et al.  Firing rate and recruitment order of toe extensor motor units in different modes of voluntary conraction. , 1977, The Journal of physiology.

[3]  R. Enoka,et al.  Motor unit recruitment and bursts of activity in the surface electromyogram during a sustained contraction , 2008, Muscle & nerve.

[4]  R K Powers,et al.  Spike frequency adaptation studied in hypoglossal motoneurons of the rat. , 1995, Journal of neurophysiology.

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

[6]  Rune W. Berg,et al.  Balanced Inhibition and Excitation Drive Spike Activity in Spinal Half-Centers , 2007, Science.

[7]  R. Gorman,et al.  Forces consistent with plateau-like behaviour of spinal neurons evoked in patients with spinal cord injuries. , 2003, Brain : a journal of neurology.

[8]  B. Bigland-ritchie,et al.  Fatigue of intermittent submaximal voluntary contractions: central and peripheral factors. , 1986, Journal of applied physiology.

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

[10]  R. Enoka,et al.  Rate coding is compressed but variability is unaltered for motor units in a hand muscle of old adults. , 2007, Journal of neurophysiology.

[11]  Alexander Adam,et al.  Recruitment order of motor units in human vastus lateralis muscle is maintained during fatiguing contractions. , 2003, Journal of neurophysiology.

[12]  L. Griffin,et al.  Motor unit discharge rate is not associated with muscle relaxation time in sustained submaximal contractions in humans , 1997, Neuroscience Letters.

[13]  P. Matthews Relationship of firing intervals of human motor units to the trajectory of post‐spike after‐hyperpolarization and synaptic noise. , 1996, The Journal of physiology.

[14]  D. Stuart,et al.  Does motoneuron adaptation contribute to muscle fatigue? , 2007, Muscle & nerve.

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

[16]  G. Kamen,et al.  Evidence of self-sustained motoneuron firing in young and older adults. , 2005, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[17]  D. Burke,et al.  Sustained contractions produced by plateau‐like behaviour in human motoneurones , 2002, The Journal of physiology.

[18]  J. Hannerz,et al.  Discharge properties of motor units in relation to recruitment order in voluntary contraction. , 1974, Acta physiologica Scandinavica.

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

[20]  S. Gandevia,et al.  Responses of Human Motoneurons to Corticospinal Stimulation during Maximal Voluntary Contractions and Ischemia , 2003, The Journal of Neuroscience.

[21]  S. Murakami,et al.  Motor unit activities during maintained voluntary muscle contraction at constant levels in man , 1981, Neuroscience Letters.

[22]  C. D. De Luca,et al.  Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions. , 2005, Journal of applied physiology.

[23]  D. Kernell,et al.  Time course and properties of late adaptation in spinal motoneurones of the cat , 2004, Experimental Brain Research.

[24]  W. Rymer,et al.  Windup of flexion reflexes in chronic human spinal cord injury: a marker for neuronal plateau potentials? , 2003, Journal of neurophysiology.

[25]  G. A. Robinson,et al.  Task and fatigue effects on low-threshold motor units in human hand muscle. , 1989, Journal of neurophysiology.

[26]  J. Borg,et al.  Firing properties of single human motor units on maintained maximal voluntary effort. , 1981, Ciba Foundation symposium.

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

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

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

[30]  Kelvin E. Jones,et al.  Neuronal variability: noise or part of the signal? , 2005, Nature Reviews Neuroscience.

[31]  R. Enoka,et al.  Time to failure of a sustained contraction is predicted by target torque and initial electromyographic bursts in elbow flexor muscles , 2007, Muscle & nerve.

[32]  A. Fuglevand,et al.  Cessation of human motor unit discharge during sustained maximal voluntary contraction , 1999, Neuroscience Letters.

[33]  O Kiehn,et al.  Serotonin‐induced bistability of turtle motoneurones caused by a nifedipine‐sensitive calcium plateau potential. , 1989, The Journal of physiology.

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

[35]  Roger M Enoka,et al.  Task differences with the same load torque alter the endurance time of submaximal fatiguing contractions in humans. , 2002, Journal of neurophysiology.

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

[37]  P. Schwindt,et al.  Properties of a persistent inward current in normal and TEA-injected motoneurons. , 1980, Journal of neurophysiology.

[38]  B. Maton,et al.  The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study , 2004, European Journal of Applied Physiology and Occupational Physiology.

[39]  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.

[40]  B. Maton,et al.  The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study , 2004, European Journal of Applied Physiology and Occupational Physiology.

[41]  J. Duchateau,et al.  Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus , 2001, The Journal of physiology.