Structural differentiation of skeletal muscle fibers in the absence of innervation in humans

The relative importance of muscle activity versus neurotrophic factors in the maintenance of muscle differentiation has been greatly debated. Muscle biopsies from spinal cord injury patients, who were trained with an innovative protocol of functional electrical stimulation (FES) for prolonged periods (2.4–9.3 years), offered the unique opportunity of studying the structural recovery of denervated fibers from severe atrophy under the sole influence of muscle activity. FES stimulation induced surprising recovery of muscle structure, mass, and force even in patients whose muscles had been denervated for prolonged periods before the beginning of FES training (up to 2 years) and had almost completely lost muscle-specific internal organization. Ninety percent (or more) of the fibers analyzed by electron microscopy showed a striking recovery of the ultrastructural organization of myofibrils and Ca2+-handling membrane systems. This functional/structural restoration follows a pattern that mimics some aspects of normal muscle differentiation. Most importantly, the recovery occurs in the complete absence of motor and sensory innervation and of nerve-derived trophic factors, that is, solely under the influence of muscle activity induced by electrical stimulation.

[1]  J. Eccles,et al.  The action potentials of the alpha motoneurones supplying fast and slow muscles , 1958, The Journal of physiology.

[2]  J. Eccles,et al.  Differentiation of fast and slow muscles in the cat hind limb , 1960, The Journal of physiology.

[3]  J. E. Bateman Trauma to nerves in limbs , 1962 .

[4]  G. Vrbóva The effect of motoneurone activity on the speed of contraction of striated muscle , 1963, The Journal of physiology.

[5]  C. Pellegrino,et al.  AN ELECTRON MICROSCOPE STUDY OF DENERVATION ATROPHY IN RED AND WHITE SKELETAL MUSCLE FIBERS , 1963, The Journal of cell biology.

[6]  G. J. Romanes,et al.  Current Problems of Lower Vertebrate Phylogeny. , 1969 .

[7]  S Salmons,et al.  The influence of activity on some contractile characteristics of mammalian fast and slow muscles , 1969, The Journal of physiology.

[8]  Norway,et al.  Contractile properties of muscle: control by pattern of muscle activity in the rat , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[9]  B. Eisenberg,et al.  Discrimination between fiber populations in mammalian skeletal muscle by using ultrastructural parameters. , 1976, Journal of ultrastructure research.

[10]  K. Schimrigk,et al.  The effect of electrical stimulation on the experimentally denervated rat muscle. , 1977, Scandinavian journal of rehabilitation medicine.

[11]  K. Angquist,et al.  Z- and M-band appearance in different histochemically defined types of human skeletal muscle fibers. , 1982, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[12]  T. Lømo,et al.  Slow‐to‐fast transformation of denervated soleus muscles by chronic high‐frequency stimulation in the rat. , 1988, The Journal of physiology.

[13]  H. Blau,et al.  Differentiation of fiber types in aneural musculature of the prenatal rat hindlimb. , 1990, Developmental biology.

[14]  R. Waters,et al.  Definition of complete spinal cord injury , 1991, Paraplegia.

[15]  F. Rieger,et al.  Muscle fibers from dysgenic mouse in vivo lack a surface component of peripheral couplings. , 1991, Developmental biology.

[16]  J. Hoh,et al.  Myogenic regulation of mammalian skeletal muscle fibres. , 1991, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[17]  C. Franzini-armstrong,et al.  Abnormal junctions between surface membrane and sarcoplasmic reticulum in skeletal muscle with a mutation targeted to the ryanodine receptor. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A D Grinnell,et al.  Dynamics of nerve-muscle interaction in developing and mature neuromuscular junctions. , 1995, Physiological reviews.

[19]  B. Carlson,et al.  Electron microscopic study of long‐term denervated rat skeletal muscle , 1997, The Anatomical record.

[20]  M. Devivo,et al.  Recent trends in mortality and causes of death among persons with spinal cord injury. , 1999, Archives of physical medicine and rehabilitation.

[21]  S Sauermann,et al.  Basic design and construction of the Vienna FES implants: existing solutions and prospects for new generations of implants. , 2001, Medical engineering & physics.

[22]  B. Carlson,et al.  Reparative myogenesis in long‐term denervated skeletal muscles of adult rats results in a reduction of the satellite cell population , 2001, The Anatomical record.

[23]  Christian Hofer,et al.  A stimulator for functional activation of denervated muscles. , 2002, Artificial organs.

[24]  V. Edgerton,et al.  Adaptations in skeletal muscle disuse or decreased-use atrophy. , 2002, American journal of physical medicine & rehabilitation.

[25]  G. Vrbóva,et al.  Effects of long-term electrical stimulation on some contractile and metabolic characteristics of fast rabbit muscles , 1973, Pflügers Archiv.

[26]  C. Franzini-armstrong,et al.  Differentiation of membrane systems during development of slow and fast skeletal muscle fibres in chicken , 1993, Journal of Muscle Research & Cell Motility.

[27]  R. Triolo,et al.  Clinical Applications of Electrical Stimulation After Spinal Cord Injury , 2004, The journal of spinal cord medicine.

[28]  Stanley Salmons,et al.  The reorganization of subcellular structure in muscle undergoing fast-to-slow type transformation , 1981, Cell and Tissue Research.

[29]  H. Kern,et al.  Long‐Term Denervation in Humans Causes Degeneration of Both Contractile and Excitation‐Contraction Coupling Apparatus, Which Is Reversible by Functional Electrical Stimulation (FES): A Role for Myofiber Regeneration? , 2004, Journal of neuropathology and experimental neurology.

[30]  B. Carlson,et al.  Contractile and histochemical properties of regenerating cross-transplanted fast and slow muscles in the rat , 2004, Pflügers Archiv.

[31]  A. Tessler,et al.  Spinal shock revisited: a four-phase model , 2004, Spinal Cord.

[32]  Christian Hofer,et al.  Electrical stimulation of denervated muscles: first results of a clinical study. , 2005, Artificial organs.

[33]  P. Peckham,et al.  Functional electrical stimulation for neuromuscular applications. , 2005, Annual review of biomedical engineering.

[34]  S. Boncompagni,et al.  Progressive disorganization of the excitation-contraction coupling apparatus in aging human skeletal muscle as revealed by electron microscopy: a possible role in the decline of muscle performance. , 2006, The journals of gerontology. Series A, Biological sciences and medical sciences.

[35]  M. Devivo,et al.  Trends in life expectancy after spinal cord injury. , 2006, Archives of physical medicine and rehabilitation.