The innervation and organization of motor units in a series-fibered human muscle: the brachioradialis.

We studied the innervation and organization of motor units in the brachioradialis muscle of 25 normal human subjects. We recorded intramuscular EMG signals at points separated by 15 mm along the proximodistal muscle axis during moderate isometric contractions, identified from 27 to 61 (mean 39) individual motor units per subject using EMG decomposition, and estimated the locations of the endplates and distal muscle/tendon junctions from the motor-unit action potential (MUAP) propagation patterns and terminal standing waves. In three subjects all the motor units were innervated in a single endplate zone. In the other 22 subjects, the motor units were innervated in 3-6 (mean 4) distinct endplate zones separated by 15-55 mm along the proximodistal axis. One-third of the motor units had fibers innervated in more than one zone. The more distally innervated motor units had distinct terminal waves indicating tendonous termination, while the more proximal motor units lacked terminal waves, indicating intrafascicular termination. Analysis of blocked MUAP components revealed that 19% of the motor units had at least one doubly innervated fiber, i.e., a fiber innervated in two different endplate zones by two different motoneurons, and thus belonging to two different motor units. These results are consistent with the brachioradialis muscle having a series-fibered architecture consisting of multiple, overlapping bands of muscle fibers in most individuals and a simple parallel-fibered architecture in some individuals.

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

[2]  P. Sheard,et al.  Examination of intrafascicular muscle fiber terminations: Implications for tension delivery in series‐fibered muscles , 2000, Journal of morphology.

[3]  D. Farina,et al.  Estimation of single motor unit conduction velocity from surface electromyogram signals detected with linear electrode arrays , 2001, Medical and Biological Engineering and Computing.

[4]  C. Gans,et al.  Serially arranged myofibers: An unappreciated variant in muscle architecture , 1992, Experientia.

[5]  G. I. Taylor,et al.  A Comparative Anatomical Study of Brachioradialis and Flexor Carpi Ulnaris Muscles: Implications for Total Tongue Reconstruction , 2008, Plastic and reconstructive surgery.

[6]  T. English,et al.  Anatomical and Physiological Considerations , 1992 .

[7]  Paul W Hodges,et al.  Muscle Fiber and Motor Unit Behavior in the Longest Human Skeletal Muscle , 2005, The Journal of Neuroscience.

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

[9]  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.

[10]  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.

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

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

[13]  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.

[14]  C. Sherrington,et al.  Numbers and Contraction-Values of Individual Motor-Units Examined in some Muscles of the Limb , 1930 .

[15]  R L Lieber,et al.  Anatomy of the radial nerve motor branches in the forearm. , 1997, The Journal of hand surgery.

[16]  R Merletti,et al.  Location of innervation zones of sternocleidomastoid and scalene muscles – a basis for clinical and research electromyography applications , 2002, Clinical Neurophysiology.

[17]  C. Disselhorst-Klug,et al.  Principles of high-spatial-resolution surface EMG (HSR-EMG): single motor unit detection and application in the diagnosis of neuromuscular disorders. , 1997, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[18]  Karin Roeleveld,et al.  Motor unit size estimation of enlarged motor units with surface electromyography , 1998, Muscle & nerve.

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

[20]  T. Hijikata,et al.  Functional morphology of serially linked skeletal muscle fibers. , 1997, Acta anatomica.

[21]  V. Edgerton,et al.  Role of motor unit structure in defining function , 2001, Muscle & nerve.

[22]  T. Masuda,et al.  Innervation zones of the upper and lower limb muscles estimated by using multichannel surface EMG. , 2000, Journal of human ergology.

[23]  Kevin C McGill,et al.  Increased jitter and blocking in normal muscles due to doubly innervated muscle fibers , 2003, Muscle & nerve.

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

[25]  V G Macefield,et al.  Comparison of contractile properties of single motor units in human intrinsic and extrinsic finger muscles , 2000, The Journal of physiology.

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

[27]  S. Wray.  Innervation ratios for large and small limb muscles in the baboon , 1969, The Journal of comparative neurology.

[28]  P W Sheard.  Tension Delivery from Short Fibers in Long Muscles , 2000, Exercise and sport sciences reviews.

[29]  D. Farina,et al.  Analysis of motor units with high-density surface electromyography. , 2008, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

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

[31]  F. Richmond,et al.  Fiber architecture and histochemistry in the cat neck muscle, biventer cervicis. , 1988, Journal of neurophysiology.

[32]  K. McGill,et al.  Electrophysiological evidence of doubly innervated branched muscle fibers in the human brachioradialis muscle , 2007, Clinical Neurophysiology.

[33]  G. Loeb,et al.  Architecture and consequent physiological properties of the semitendinosus muscle in domestic goats , 1989, Journal of morphology.

[34]  Robert Oostenveld,et al.  Topographical characteristics of motor units of the lower facial musculature revealed by means of high-density surface EMG. , 2006, Journal of neurophysiology.

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

[36]  E. Hall‐Craggs,et al.  Neuromuscular relationships in a muscle having segregated motor endplate zones. I. Anatomical and physiological considerations , 1986, The Journal of comparative neurology.

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

[38]  Kevin C. McGill,et al.  Satellite potentials of motor unit action potentials in normal muscles: a new hypothesis for their origin , 1999, Clinical Neurophysiology.

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

[40]  A W Toga,et al.  Physiological and developmental implications of motor unit anatomy. , 1991, Journal of neurobiology.

[41]  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.

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

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

[44]  T. Masuda,et al.  The propagation of motor unit action potential and the location of neuromuscular junction investigated by surface electrode arrays. , 1983, Electroencephalography and clinical neurophysiology.

[45]  A. Dalley,et al.  Nerve supply of the brachioradialis muscle: Surgically relevant variations of the extramuscular branches of the radial nerve , 2005, Clinical anatomy.

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

[47]  S. Delp,et al.  Upper limb muscle volumes in adult subjects. , 2007, Journal of biomechanics.

[48]  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.

[49]  C Gans,et al.  Muscle architecture and control demands. , 1992, Brain, behavior and evolution.

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

[51]  Organization of single motor units in feline sartorius. , 1994, Journal of neurophysiology.

[52]  F. Richmond,et al.  Muscle-fiber compartmentalization in cat splenius muscles. , 1985, Journal of neurophysiology.

[53]  P. H. Kleinpenning,et al.  The equivalent source description representing the extinction of an action potential at a muscle fiber ending. , 1990, Mathematical biosciences.

[54]  Alan J. Sokoloff,et al.  Neuromuscular Organization of the Superior Longitudinalis Muscle in the Human Tongue , 2006, Cells Tissues Organs.

[55]  A J Fuglevand,et al.  Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation. , 1996, Journal of neurophysiology.