Motoneurons: A preferred firing range across vertebrate species?

The term “preferred firing range” describes a pattern of human motor unit (MU) unitary discharge during a voluntary contraction in which the profile of the spike‐frequency of the MU's compound action potential is dissociated from the profile of the presumed depolarizing pressure exerted on the unit's spinal motoneuron (MN). Such a dissociation has recently been attributed by inference to the presence of a plateau potential (PP) in the active MN. This inference is supported by the qualitative similarities between the firing pattern of human MUs during selected types of relatively brief muscle contraction and that of intracellularly stimulated, PP‐generating cat MNs in a decerebrate preparation, and turtle MNs in an in vitro slice of spinal cord. There are also similarities between the stimulus‐response behavior of intracellularly stimulated turtle MNs and human MUs during the elaboration of a slowly rising voluntary contraction. This review emphasizes that there are a variety of open issues concerning the PP. Nonetheless, a rapidly growing body of comparative vertebrate evidence supports the idea that the PP and other forms of non‐linear MN behavior play a major role in the regulation of muscle force, from the lamprey to the human. © 2002 Wiley Periodicals, Inc. Muscle Nerve 25: 000–000, 2002

[1]  Jaynie F. Yang,et al.  Self-sustained firing of human motor units , 1998, Neuroscience Letters.

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

[3]  S C Gandevia,et al.  Large Involuntary Forces Consistent with Plateau-Like Behavior of Human Motoneurons , 2001, The Journal of Neuroscience.

[4]  B A Conway,et al.  Plateau potentials in alpha‐motoneurones induced by intravenous injection of L‐dopa and clonidine in the spinal cat. , 1988, The Journal of physiology.

[5]  S. Iversen Motor control , 2000, Clinical Neurophysiology.

[6]  S. Grillner,et al.  Inhibition of N- and L-type Ca2+ currents by dopamine in lamprey spinal motoneurons. , 1999, Neuroreport.

[7]  J. Hounsgaard,et al.  NMDA-Induced intrinsic voltage oscillations depend on L-type calcium channels in spinal motoneurons of adult turtles. , 1998, Journal of neurophysiology.

[8]  J. Hounsgaard,et al.  Non-volatile general anaesthetics reduce spinal activity by suppressing plateau potentials , 1999, Neuroscience.

[9]  A. Gydikov,et al.  Physiological Characteristics of the Tonic and Phasic Motor Units in Human Muscles , 1973 .

[10]  T. Eken Spontaneous electromyographic activity in adult rat soleus muscle. , 1998, Journal of neurophysiology.

[11]  Transmitter regulation of plateau properties in turtle motoneurons. , 1998, Journal of neurophysiology.

[12]  Adapting motoneurons for motor behavior. , 1999, Progress in brain research.

[13]  H Hultborn,et al.  Short-term plasticity in hindlimb motoneurons of decerebrate cats. , 1998, Journal of neurophysiology.

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

[15]  J. Coast Handbook of Physiology. Section 12. Exercise: Regulation and Integration of Multiple Systems , 1997 .

[16]  M. Gorassini,et al.  Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. , 2001, Journal of neurophysiology.

[17]  P. Schwindt,et al.  A persistent negative resistance in cat lumbar motoneurons , 1977, Brain Research.

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

[19]  C. C. A. M. Gielen,et al.  The relative activation of muscles during isometric contractions and low-velocity movements against a load , 1994, Experimental Brain Research.

[20]  H. Wigström,et al.  Maintained changes in motoneuronal excitability by short‐lasting synaptic inputs in the decerebrate cat. , 1988, The Journal of physiology.

[21]  G. L. Soderberg,et al.  The effect of muscle length on motor unit discharge characteristics in human tibialis anterior muscle , 2004, Experimental Brain Research.

[22]  D. Cj Decomposition of the EMG signal into constituent motor unit action potentials. , 1995 .

[23]  C. D. De Luca Decomposition of the EMG signal into constituent motor unit action potentials. , 1995, Muscle & nerve.

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

[25]  R. Russo,et al.  Dynamics of intrinsic electrophysiological properties in spinal cord neurones. , 1999, Progress in biophysics and molecular biology.

[26]  J. Duchateau,et al.  Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans , 1998, The Journal of physiology.

[27]  S. Grillner,et al.  Activation of NMDA receptors elecits fictive locomotion and bistable membrane properties in the lamprey spinal cord , 1985, Brain Research.

[28]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. , 1980, The Journal of physiology.

[29]  R. Keynes The ionic channels in excitable membranes. , 1975, Ciba Foundation symposium.

[30]  D. Kosarov,et al.  Dependence of the discharge frequency of motor units in different human muscles upon the level of the isometric muscle tension. , 1976, Electromyography and clinical neurophysiology.

[31]  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.

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

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

[34]  O. Kiehn,et al.  Functional role of plateau potentials in vertebrate motor neurons , 1998, Current Opinion in Neurobiology.

[35]  R. Reinking,et al.  Properties of spinal motoneurons and interneurons in the adult turtle: Provisional classification by cluster analysis , 1998, The Journal of comparative neurology.

[36]  P Bawa,et al.  Repetitive doublets in human flexor carpi radialis muscle. , 1983, The Journal of physiology.

[37]  C. C. A. M. Gielen,et al.  The relation between the direction dependence of electromyographic amplitude and motor unit recruitment thresholds during isometric contractions , 1994, Experimental Brain Research.

[38]  R. Eckert,et al.  A non-inactivating inward current recorded during small depolarizing voltage steps in snail pacemaker neurons , 1975, Brain Research.

[39]  P. Cavallari,et al.  Motor neuron 'bistability'. A pathogenetic mechanism for cramps and myokymia. , 1994, Brain : a journal of neurology.

[40]  A. De Luca,et al.  Changes of membrane electrical properties in extensor digitorum longus muscle from dystrophic (mdx) mice , 1995, Muscle & nerve.

[41]  R. Brownstone,et al.  An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks , 1999, Brain Research.

[42]  C A Del Negro,et al.  Ionic basis for serotonin-induced bistable membrane properties in guinea pig trigeminal motoneurons. , 1998, Journal of neurophysiology.

[43]  H Hultborn Plateau potentials and their role in regulating motoneuronal firing. , 1999, Progress in brain research.

[44]  D. Winter,et al.  Models of recruitment and rate coding organization in motor-unit pools. , 1993, Journal of neurophysiology.

[45]  A J Fuglevand,et al.  Force-frequency and fatigue properties of motor units in muscles that control digits of the human hand. , 1999, Journal of neurophysiology.

[46]  M. Gorassini,et al.  Spasticity in rats with sacral spinal cord injury. , 1999, Journal of neurotrauma.

[47]  M. Gola Neurones à ondes-salves des mollusques , 1974, Pflügers Archiv.

[48]  O. Kiehn,et al.  Selective depletion of spinal monoamines changes the rat soleus EMG from a tonic to a more phasic pattern. , 1996, The Journal of physiology.

[49]  P. Schwindt,et al.  Multiple actions of N-methyl-d-aspartate on cat neocortical neurons in vitro , 1983, Brain Research.

[50]  S Grillner,et al.  GABAB receptor activation causes a depression of low- and high-voltage-activated Ca2+ currents, postinhibitory rebound, and postspike afterhyperpolarization in lamprey neurons. , 1993, Journal of neurophysiology.

[51]  P H Ellaway,et al.  Modulation of single motor unit discharges using magnetic stimulation of the motor cortex in incomplete spinal cord injury , 2000, Journal of neurology, neurosurgery, and psychiatry.

[52]  Toyohiro Akiyama,et al.  Pacemaker Potentials for the Periodic Burst Discharge in the Heart Ganglion of a Stomatopod, Squilla oratoria , 1967, The Journal of general physiology.

[53]  J. Hounsgaard,et al.  l-Type calcium channels but not N-methyl-d-aspartate receptor channels mediate rhythmic activity induced by cholinergic agonist in motoneurons from turtle spinal cord slices , 1999, Neuroscience Letters.

[54]  R. Eckert,et al.  A voltage‐sensitive persistent calcium conductance in neuronal somata of Helix. , 1976, The Journal of physiology.

[55]  J. Hounsgaard,et al.  Depolarization-induced facilitation of a plateau-generating current in ventral horn neurons in the turtle spinal cord. , 1997, Journal of neurophysiology.

[56]  Membrane potential changes of phrenic motoneurons during fictive vomiting, coughing, and swallowing in the decerebrate cat. , 1992, Journal of neurophysiology.

[57]  R. Russo,et al.  Short-term plasticity in turtle dorsal horn neurons mediated by L-type Ca2+ channels , 1994, Neuroscience.

[58]  C. Heckman,et al.  The Physiological Control of Motoneuron Activity , 1996 .

[59]  S. Weidmann,et al.  Effect of current flow on the membrane potential of cardiac muscle , 1951, The Journal of physiology.

[60]  O Kiehn,et al.  Response properties of motoneurones in a slice preparation of the turtle spinal cord. , 1988, The Journal of physiology.

[61]  A Kossev,et al.  Discharge pattern of human motor units during dynamic concentric and eccentric contractions. , 1998, Electroencephalography and clinical neurophysiology.

[62]  A. Willem Monster,et al.  Firing rate behavior of human motor units during isometric voluntary contraction: relation to unit size , 1979, Brain Research.

[63]  P. Schwindt,et al.  Effects of barium on cat spinal motoneurons studied by voltage clamp. , 1980, Journal of neurophysiology.

[64]  P H Ellaway,et al.  Responses of thenar muscles to transcranial magnetic stimulation of the motor cortex in patients with incomplete spinal cord injury , 1998, Journal of neurology, neurosurgery, and psychiatry.

[65]  J. Hounsgaard,et al.  Ca++ dependent bistability induced by serotonin in spinal motoneurons , 2004, Experimental Brain Research.

[66]  J. Buchanan The roles of spinal interneurons and motoneurons in the lamprey locomotor network. , 1999, Progress in brain research.

[67]  H. Hultborn,et al.  Voltage-dependent excitation of motoneurones from spinal locomotor centres in the cat , 2004, Experimental Brain Research.

[68]  S. Grillner,et al.  N-methyl-D-aspartate receptor-induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  P. Stein,et al.  Cutaneous stimulation evokes long-lasting excitation of spinal interneurons in the turtle. , 1990, Journal of neurophysiology.

[70]  R. Brownstone,et al.  Characterization of calcium currents in functionally mature mouse spinal motoneurons , 2000, The European journal of neuroscience.

[71]  J. Hounsgaard,et al.  Calcium conductance and firing properties of spinal motoneurones in the turtle. , 1988, The Journal of physiology.

[72]  C. Heckman,et al.  Influence of voltage-sensitive dendritic conductances on bistable firing and effective synaptic current in cat spinal motoneurons in vivo. , 1996, Journal of neurophysiology.

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

[74]  M. Binder,et al.  Multiple mechanisms of spike-frequency adaptation in motoneurones , 1999, Journal of Physiology-Paris.

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

[76]  P. Schwindt,et al.  Role of a persistent inward current in motoneuron bursting during spinal seizures. , 1980, Journal of neurophysiology.

[77]  H Hultborn,et al.  Possible functions of transmitter-controlled plateau potentials in alpha motoneurones. , 1989, Progress in brain research.

[78]  M. Siu,et al.  Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. , 2001, Journal of neurophysiology.

[79]  S. Currie,et al.  Sensory-evoked pocket scratch motor patterns in the in vitro turtle spinal cord: reduction of excitability by an N-methyl-D-aspartate antagonist. , 1996, Journal of neurophysiology.

[80]  Jørn Hounsgaard,et al.  Chapter 5 Adapting Motoneurons for Motor Behavior , 1999 .

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

[82]  O. Kiehn Plateau potentials and active integration in the ‘final common pathway’ for motor behaviour , 1991, Trends in Neurosciences.

[83]  K Kanosue,et al.  The number of active motor units and their firing rates in voluntary contraction of human brachialis muscle. , 1979, The Japanese journal of physiology.

[84]  C. Heckman,et al.  Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. , 1998, Journal of neurophysiology.

[85]  Pierre A Guertin,et al.  Chemical and electrical stimulation induce rhythmic motor activity in an in vitro preparation of the spinal cord from adult turtles , 1998, Neuroscience Letters.

[86]  L. M. Jordan,et al.  On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat , 1992, Experimental Brain Research.

[87]  C. G. Phillips,et al.  Differentiation of tonic from phasic alpha ventral horn cells by stretch, pinna and crossed extensor reflexes. , 1957, Journal of neurophysiology.

[88]  ter Bm Bart Haar Romeny,et al.  Behaviour of motor units of human arm muscles: differences between slow isometric contraction and relaxation , 1985 .

[89]  S. Grillner,et al.  On the cellular bases of vertebrate locomotion. , 1999, Progress in brain research.

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

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

[92]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. , 1980, The Journal of physiology.

[93]  I. Nagaoka,et al.  Effect of vitamin K3 on macrophage functions and intracellular calcium. , 1988, Comparative biochemistry and physiology. A, Comparative physiology.

[94]  D F Russell,et al.  Special cellular and synaptic mechanisms in motor pattern generation. , 1988, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.

[95]  C. Heckman,et al.  Synaptic integration in bistable motoneurons. , 1999, Progress in brain research.

[96]  Ole Kiehn,et al.  Chapter 21 Possible functions of transmitter-controlled plateau potentials in α motoneurones , 1989 .

[97]  Robert H. Lee,et al.  The role of voltage-sensitive dendritic conductances in generating bistable firing patterns in motoneurons , 1999, Journal of Physiology-Paris.

[98]  M. Gorassini,et al.  Activity of hindlimb motor units during locomotion in the conscious rat. , 2000, Journal of neurophysiology.

[99]  G Kamen,et al.  Motor unit discharge behavior in older adults during maximal-effort contractions. , 1995, Journal of applied physiology.

[100]  E. Pierrot-Deseilligny,et al.  Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneurons , 1996, Progress in Neurobiology.

[101]  P. Stein,et al.  Spinal Motor Patterns in the Turtle a , 1998, Annals of the New York Academy of Sciences.

[102]  N W Daw,et al.  The role of NMDA receptors in information processing. , 1993, Annual review of neuroscience.

[103]  P. Stein,et al.  Glutamate antagonists applied to midbody spinal cord segments reduce the excitability of the fictive rostral scratch reflex in the turtle , 1992, Brain Research.

[104]  R. Katz,et al.  Recurrent inhibition in humans , 1999, Progress in Neurobiology.

[105]  D. F. Russell,et al.  Slow active potentials and bursting motor patterns in pyloric network of the lobster, Panulirus interruptus. , 1982, Journal of neurophysiology.

[106]  H. Wigström,et al.  Prolonged activation of soleus motoneurones following a conditioning train in soleus Ia afferents — A case for a reverberating loop? , 1975, Neuroscience Letters.

[107]  C J De Luca,et al.  Motor control of low-threshold motor units in the human trapezius muscle. , 2001, Journal of neurophysiology.

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

[109]  M. Gorassini,et al.  Activation patterns of hindlimb motor units in the awake rat and their relation to motoneuron intrinsic properties. , 1999, Journal of neurophysiology.

[110]  T. Hornby Neuromodulation of the intrinsic stimulus current-spike frequency relationship of spinal motoneurons in the adult turtle , 2000 .

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

[112]  D. F. Russell,et al.  Bursting neural networks: a reexamination. , 1978, Science.

[113]  Kazunori Yasuda,et al.  Behavior of single motor units of human tibialis anterior muscle during voluntary shortening contraction under constant load torque , 1985, Experimental Neurology.

[114]  D. Mazevet,et al.  The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[115]  P J Delwaide,et al.  Absence of response to early transcranial magnetic stimulation in ischemic stroke patients: prognostic value for hand motor recovery. , 1999, Stroke.

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

[117]  J. Hounsgaard,et al.  Intrinsic membrane properties causing a bistable behaviour of α-motoneurones , 2004, Experimental Brain Research.

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

[119]  S. Boniface,et al.  Origin of the secondary increase in firing probability of human motor neurons following transcranial magnetic stimulation. Studies in healthy subjects, type I hereditary motor and sensory neuropathy and multiple sclerosis. , 1991, Brain : a journal of neurology.

[120]  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.

[121]  P. Schwindt,et al.  Calcium currents in acutely isolated human neocortical neurons. , 1993, Journal of neurophysiology.

[122]  L M Jordan,et al.  Dendritic L‐type calcium currents in mouse spinal motoneurons: implications for bistability , 2000, The European journal of neuroscience.

[123]  O Kiehn,et al.  Bistable firing properties of soleus motor units in unrestrained rats. , 1989, Acta physiologica Scandinavica.

[124]  S. Grillner,et al.  Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. , 1989, Journal of neurophysiology.

[125]  Hans Hultborn,et al.  Plateau potentials and their role in regulating motoneuronal firing. , 2002, Advances in experimental medicine and biology.

[126]  J. Duchateau,et al.  Effects of immobilization on contractile properties, recruitment and firing rates of human motor units. , 1990, The Journal of physiology.