Muscle Fiber and Motor Unit Behavior in the Longest Human Skeletal Muscle

The sartorius muscle is the longest muscle in the human body. It is strap-like, up to 600 mm in length, and contains five to seven neurovascular compartments, each with a neuromuscular endplate zone. Some of its fibers terminate intrafascicularly, whereas others may run the full length of the muscle. To assess the location and timing of activation within motor units of this long muscle, we recorded electromyographic potentials from multiple intramuscular electrodes along sartorius muscle during steady voluntary contraction and analyzed their activity with spike-triggered averaging from a needle electrode inserted near the proximal end of the muscle. Approximately 30% of sartorius motor units included muscle fibers that ran the full length of the muscle, conducting action potentials at 3.9 ± 0.1 m/s. Most motor units were innervated within a single muscle endplate zone that was not necessarily near the midpoint of the fiber. As a consequence, action potentials reached the distal end of a unit as late as 100 ms after initiation at an endplate zone. Thus, contractile activity is not synchronized along the length of single sartorius fibers. We postulate that lateral transmission of force from fiber to endomysium and a wide distribution of motor unit endplates along the muscle are critical for the efficient transmission of force from sarcomere to tendon and for the prevention of muscle injury caused by overextension of inactive regions of muscle fibers.

[1]  K. McDonald,et al.  Eccentric contraction injury in dystrophic canine muscle. , 2002, Archives of physical medicine and rehabilitation.

[2]  E Eldred,et al.  Tapering of the intrafascicular endings of muscle fibers and its implications to relay of force , 1993, The Anatomical record.

[3]  G. Liu,et al.  Duchenne muscular dystrophy: MR grading system with functional correlation. , 1993, Radiology.

[4]  P Huijing,et al.  Muscular force transmission: a unified, dual or multiple system? A review and some explorative experimental results. , 1999, Archives of physiology and biochemistry.

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

[6]  Stephen J. Kaufman,et al.  Localization of α7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles , 2002, Cell and Tissue Research.

[7]  A. Lamminen,et al.  Magnetic resonance imaging of primary skeletal muscle diseases: patterns of distribution and severity of involvement. , 1990, The British journal of radiology.

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

[9]  R L Lieber,et al.  12 Force Transmission in Skeletal Muscle: from Actomyosin to External Tendons , 1997, Exercise and sport sciences reviews.

[10]  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.

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

[12]  D. Morgan From sarcomeres to whole muscles. , 1985, The Journal of experimental biology.

[13]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[14]  S. Morris,et al.  The sartorius muscle: anatomic considerations for reconstructive surgeons , 2005, Surgical and Radiologic Anatomy.

[15]  Lars Arendt-Nielsen,et al.  Conduction velocity of motor unit action potentials in human anterior tibial muscle as a new size principle parameter , 1987 .

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

[17]  M Miyashita,et al.  Muscle fiber conduction velocity related to stimulation rate. , 1989, Electroencephalography and clinical neurophysiology.

[18]  M. Johnson,et al.  Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. , 1973, Journal of the neurological sciences.

[19]  S. Street,et al.  Lateral transmission of tension in frog myofibers: A myofibrillar network and transverse cytoskeletal connections are possible transmitters , 1983, Journal of cellular physiology.

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

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

[22]  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.

[23]  P. Huijing,et al.  Myofascial Force Transmission Causes Interaction between Adjacent Muscles and Connective Tissue: Effects of Blunt Dissection and Compartmental Fasciotomy on Length Force Characteristics of Rat Extensor Digitorum Longus Muscle , 2001, Archives of physiology and biochemistry.

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