Electrophysiological evidence of adult human skeletal muscle fibres with multiple endplates and polyneuronal innervation

Electromyographic (EMG) signals were recorded using intramuscular electrodes at six different sites in the brachioradialis muscles during voluntary isometric contractions in four subjects. The potential waveforms and discharge patterns of up to 12 simultaneously active motor units were identified from each signal using computer‐aided decomposition. Out of a total of 301 motor unit potentials identified, 23 potentials exhibited behaviour consistent with having been generated by muscle fibres that were innervated by two different motoneurons at widely separated endplates. These potentials discharged in association with two different motor units, but were blocked or delayed whenever the two motor units discharged within a few milliseconds of one another. The blocking was consistent with a collision or refractoriness when one motoneuron tried to excite the fibre while it was already conducting an action potential initiated by the other motoneuron. The delays were consistent with decreased conduction velocity associated with incomplete recovery of the fibre after a preceding action potential. From the temporal separation between the discharges of the two motoneurons that resulted in blocking, the spatial separation between the endplates was estimated to be between 26 and 44 mm. These findings challenge the classical concept of the motor unit as an anatomically distinct and functionally independent entity. It is suggested that the human brachioradialis muscle may contain both long, polyneuronally innervated fibres and short, serially linked, singly innervated fibres.

[1]  Kevin C. McGill,et al.  Optimal resolution of superimposed action potentials , 2002, IEEE Transactions on Biomedical Engineering.

[2]  G. Vrbóva,et al.  Activity-dependent interactions between motoneurones and muscles: Their role in the development of the motor unit , 1993, Progress in Neurobiology.

[3]  P. Sheard,et al.  Formation of new myotubes occurs exclusively at the multiple innervation zones of an embryonic large muscle , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[4]  S. W. Kuffler,et al.  MULTIPLE MOTOR INNERVATION OF THE FROG'S SARTORIUS MUSCLE , 1941 .

[5]  Håkan Askmark,et al.  Topographical localization of motor endplates in cryosections of whole human muscles , 1984, Muscle & nerve.

[6]  F BUCHTHAL,et al.  REFRACTORY PERIOD AND CONDUCTION VELOCITY OF THE STRIATED MUSCLE FIBRE. , 1963, Acta physiologica Scandinavica.

[7]  F BUCHTHAL,et al.  IMPULSE PROPAGATION IN STRIATED MUSCLE FIBERS AND THE ROLE OF THE INTERNAL CURRENTS IN ACTIVATION , 1959, Annals of the New York Academy of Sciences.

[8]  J. Jansen,et al.  The fate of foreign endplates in cross-innervated rat soleus muscle , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[9]  G Freilinger,et al.  Human facial muscles: Dimensions, motor endplate distribution, and presence of muscle fibers with multiple motor endplates , 1997, The Anatomical record.

[10]  L. Hammarström,et al.  AUTORADIOGRAPHIC STUDIES ON THE DISTRIBUTION OF C14‐LABELLED ASCORBIC ACID AND DEHYDROASCORBIC ACID , 1966 .

[11]  G. Rossi From the pattern of human vocal muscle fibre innervation to functional remarks. , 1990, Acta oto-laryngologica. Supplementum.

[12]  A. Paul Muscle length affects the architecture and pattern of innervation differently in leg muscles of mouse, guinea pig, and rabbit compared to those of human and monkey muscles , 2001, The Anatomical record.

[13]  J. Trotter,et al.  Functional morphology of force transmission in skeletal muscle. A brief review. , 1993, Acta anatomica.

[14]  P. Merton Interaction between muscle fibres in a twitch , 1954, The Journal of physiology.

[15]  R. Balice-Gordon,et al.  Loss of Correlated Motor Neuron Activity during Synaptic Competition at Developing Neuromuscular Synapses , 2001, Neuron.

[16]  S. W. Kuffler,et al.  Motor innervation of skeletal muscle: multiple innervation of individual muscle fibres and motor unit function * , 1954, The Journal of physiology.

[17]  F BUCHTHAL,et al.  Refractory period of human muscle after the passage of a propagated action potential. , 1960, Electroencephalography and clinical neurophysiology.

[18]  E Stalberg,et al.  Propagation velocity in human muscle fibers in situ. , 1966, Acta physiologica Scandinavica. Supplementum.

[19]  C. M. Chanaud,et al.  Distribution and innervation of short, interdigitated muscle fibers in parallel‐fibered muscles of the cat hindlimb , 1987, Journal of morphology.

[20]  S. Delp,et al.  The isometric functional capacity of muscles that cross the elbow. , 2000, Journal of biomechanics.

[21]  E CHRISTENSEN,et al.  TOPOGRAPHY OF TERMINAL MOTOR INNERVATION IN STRIATED MUSCLES FROM STILLBORN INFANTS , 1959, American journal of physical medicine.

[22]  E Stålberg,et al.  Muscle fiber recovery functions studied with double pulse stimulation , 1991, Muscle & nerve.

[23]  D. Troiani,et al.  Nonlinear tension summation of different combinations of motor units in the anesthetized cat peroneus longus muscle. , 1999, Journal of neurophysiology.

[24]  Kevin C. McGill,et al.  High-Resolution Alignment of Sampled Waveforms , 1984, IEEE Transactions on Biomedical Engineering.

[25]  A. McComas,et al.  Multiple innervation of human muscle fibers , 1984, Journal of the Neurological Sciences.

[26]  D Snobl,et al.  Microarchitecture and innervation of the human latissimus dorsi muscle. , 1998, Journal of reconstructive microsurgery.

[27]  W. Zenker,et al.  Multifocal innervation and muscle length , 1990, Anatomy and Embryology.

[28]  J. L. Lilienthal,et al.  Spread of excitation in skeletal muscle; some factors contributing to the form of the electromyogram. , 1952, The American journal of physiology.

[29]  Richard R. Ribchester,et al.  Competition at silent synapses in reinnervated skeletal muscle , 2000, Nature Neuroscience.

[30]  S. Périé,et al.  Innervation of adult human laryngeal muscle fibers , 1997, Journal of the Neurological Sciences.

[31]  J. Jansen,et al.  The elimination of synapses in multiply-innervated skeletal muscle fibres of the rat: dependence on distance between end-plates , 1977, Brain Research.

[32]  B. Feinstein,et al.  Morphologic studies of motor units in normal human muscles. , 1955, Acta anatomica.

[33]  Kevin C McGill,et al.  Estimating motor-unit architectural properties by analyzing motor-unit action potential morphology , 2001, Clinical Neurophysiology.

[34]  P. Matthews,et al.  An investigation into the possible existence of polyneuronal innervation of individual skeletal muscle fibres in certain hind‐limb muscles of the cat , 1960, The Journal of physiology.

[35]  J. Fridén,et al.  Biomechanical Analysis of the Brachioradialis as a Donor in Tendon Transfer , 2001, Clinical orthopaedics and related research.

[36]  C. Sherrington Some Function Problems Attaching to Convergence , 1929, Nature.

[37]  G. Feng,et al.  Asynchronous Synapse Elimination in Neonatal Motor Units Studies Using GFP Transgenic Mice , 2001, Neuron.

[38]  J. Sanes,et al.  Development of the vertebrate neuromuscular junction. , 1999, Annual review of neuroscience.

[39]  Z C Lateva,et al.  The physiological origin of the slow afterwave in muscle action potentials. , 1997, Electroencephalography and clinical neurophysiology.

[40]  F. Richmond,et al.  In‐series fiber architecture in long human muscles , 1993, Journal of morphology.

[41]  C. Sherrington Ferrier lecture.—Some functional problems attaching to convergence , 1929 .

[42]  F. Richmond,et al.  Functional Morphology and Motor Control of Series‐Fibered Muscles , 1995, Exercise and sport sciences reviews.

[43]  A. Woolf,et al.  The innervation of muscle : a biopsy study , 1959 .

[44]  Dianne Rees BEd GradDipPhys Mcsp Nerve- Muscle Interaction , 1995 .