Fatigue pp 429-456 | Cite as

Fatigue in Adapted Systems

Overuse and Underuse Paradigms
  • T. Gordon
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 384)


Alterations in structural and biochemical properties of muscles that underlie physiological parameters of contractile force, speed and fatigability are described under conditions of 1) overuse: imposed electrical stimulation, natural exercise and functional overload; 2) reinnervation of denervated muscles; and 3) underusage: conditions of restricted use after spinal cord injury, weightlessness, immobilization and drug-induced neuromuscular blockade. These conditions demonstrate the remarkable plasticity of muscle fibers with obvious implications in health and disease. They also identify that the amount of neuromuscular activity and loading of muscle contractions are major factors determining susceptibility to fatigue and muscle strength, respectively.


Motor Unit Endurance Training Soleus Muscle Medial Gastrocnemius Apply Physiology 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alaimo MA, Smith AJL, Roy RR & Edgerton VR (1984). EMG activity of slow and fast ankle extensors following spinal cord transection. Journal of Applied Physiology 56, 1608–1613.PubMedCrossRefGoogle Scholar
  2. Alford EK, Roy RR, Hodgson JA & Edgerton VR (1989). Electromyography of rat soleus, medial gastrocnemius, and tibialis anterior during hind-limb suspension. Experimental Neurology 96, 635–649.CrossRefGoogle Scholar
  3. Allen DG, Westerblad H, Lee JA & Lannergren J (1992). Role of excitation-contraction coupling in muscle fatigue. Sports Medicine 13, 116–126.PubMedCrossRefGoogle Scholar
  4. Amphlett GW, Perry SV, Syska H, Brown M & Vrbová G (1975). Cross innervation and the regulatory protein system of rabbit soleus muscle. Nature 257, 602–604.PubMedCrossRefGoogle Scholar
  5. Andersen P & Henriksson J (1977). Training induced changes in the subgroups of human type II skeletal muscle fibers. Acta Physiology Scandinavica 99, 123–125.CrossRefGoogle Scholar
  6. Anholm JD, Stray-Gundersen J, Ramanathan M & Johnson RL Jr (1989). Sustained maximal ventilation after endurance exercise in athletes. Journal of Applied Physiology 67, 1759–1763.PubMedGoogle Scholar
  7. Antonio J & Gonyea WJ (1993). Skeletal muscle fiber hyperplasia. Medicine and Science in Sports and Exercise 25, 1333–1345.PubMedCrossRefGoogle Scholar
  8. Ariano MA, Armstrong RB & Edgerton VR (1973). Hindlimb muscle fiber populations of five mammals. Journal of Histochemistry and Cytochemistry 21, 51–55, 1973.PubMedCrossRefGoogle Scholar
  9. Ausoni S, Gorza L, Schiaffino S, Gundersen K & Lomo T (1990). expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. Journal of Neuroscience 10, 153–160.PubMedGoogle Scholar
  10. Baker JH & Matsumoto DE (1988). Adaptation of skeletal muscle to immobilization in a shortened position. Muscle & Nerve 11, 231–244.CrossRefGoogle Scholar
  11. Baldwin KM, Winder WW, Terjung RL & Holloszy J (1973). Glycolytic enzymes in different types of skeletal muscle: adaptation to exercise. American Journal of Physiology 225, 962–966.PubMedGoogle Scholar
  12. Barnard RJ & Peter JB (1969). Effect of training and exhaustion on hexokinase activity of skeletal muscle. Journal of Applied Physiology 27, 691–695.PubMedGoogle Scholar
  13. Bass A, Brdiczka D, Eyer P, Hofer S & Pette D (1969). Metabolic differentiation of distinct muscle types at the level of enzymatic organization. European Journal of Biochemistry 10, 198–206.PubMedCrossRefGoogle Scholar
  14. Bodine-Fowler SC, Roy RR Rudolph W, Haque N, Kozlovskaya IB & Edgerton VR (1992). Spaceflight and growth effects on muscle fibers in the rhesus monkey. Journal of Applied Physiology 73, 82S–89S.PubMedGoogle Scholar
  15. Bouchard C, Dionne FT, Simoneau J-A & Boulay MR (1992). Genetics of aerobic and anaerobic performances. Exercise and Sport Sciences Review 20, 27–58.Google Scholar
  16. Boutellier U, Buchel R, Kundert A & Spengler C (1992). The respiratory system as an exercise limiting factor in normal trained subjects. European Journal of Applied Physiology and Occupational Physiology 65, 347–353.PubMedCrossRefGoogle Scholar
  17. Brooks GA & Fahey TA (1985). Exercise Physiology: Human Bioenergetics and its Applications. New York: Macmillian.Google Scholar
  18. Brooks MH & Kaiser KK (1970). Three “myosin adenosine trophosphatase” systems: the nature of their pH lability and sulfhydryl dependence. Journal of Histochemistry and Cytochemistry 18, 670–672.CrossRefGoogle Scholar
  19. Brown MD, Cotter MA, Hudlická O & Vrbová G (1976). The effect of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pflügers Archiv 361, 241–250.PubMedCrossRefGoogle Scholar
  20. Buller AJ, Eccles JC & Eccles RM (1960). Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. Journal of Physiology (London) 150, 399–416.Google Scholar
  21. Burke RE (1981). Motor units: anatomy, physiology, and functional organization. In: Brookhart JM, Mountcastle VB (sec. eds.), Brooks VB (vol. ed.), Handbook of Physiology, sec. 1, vol. II, pt 1, The Nervous System: Motor Control, pp. 345-422. Bethesda, MD: American Physiological Society.Google Scholar
  22. Burke RE & Edgerton VR (1975). Motor unit properties and selective involvement in movement. Exercise and Sport Sciences Reviews 3, 31–81.PubMedCrossRefGoogle Scholar
  23. Burke RE, Levine DN, Tsairis P & Zajac FE (1973). Physiological types and histochemical profiles in motor units of the cat gastrocnemius. Journal of Physiology (London) 234, 723–748.Google Scholar
  24. Castle NA & Haylett DG (1987). Effect of channel blockers on potassium efflux from metabolically exhausted frog skeletal muscle. Journal of Physiology (London) 383, 31–43.Google Scholar
  25. Chalmers GR, Roy RR & Edgerton VR (1992). Variation and limitations in fiber enzymatic and size responses in hypertrophied muscle. Journal of Applied Physiology 73, 631–641.PubMedGoogle Scholar
  26. Chan M, Edgerton VR, Goslow GE Jr, Kurata H, Rasmussen S & Spector SA (1982). Histochemical and physiological properties of cat motor units after self-and cross-reinnervation. Journal of Physiology (London) 332, 343–361.Google Scholar
  27. Cope TC, Bodine SC, Fournier M & Edgerton VR (1986). Soleus motor units in chronic spinal transected cats: physiological and morphological alterations. Journal of Neurophysiology 55, 1202–1220.PubMedGoogle Scholar
  28. Corley K, Kowalchuk B & McComas AJ (1984). Contrasting effects of suspension on the hindlimb muscles in the hamster. Experimental Neurology 85, 30–40.PubMedCrossRefGoogle Scholar
  29. Costill DL (1986). Inside Running: Basics of Sports Physiology. Indianapolis, IN: Bechmark Press, Incorporated.Google Scholar
  30. Costill DL, Coyle EF, Dalsky G, Evans W, Fink W & Hoopes D (1977). Effects of elevated plasma FFA and insulin on muscle glycogen usage during exercise. Journal of Applied Physiology 43, 695–699.PubMedGoogle Scholar
  31. Crerar MM, Hamilton NC, Blank S, Urdea MS & Ianuzzo CD (1989). The genes for β-myosin heavy chain and glycogen phosphorylase are discoordinately regulated during compensatory growth of the plantaris muscle in the adult rat. Molecular Cellular Biochemistry 86, 115–123.CrossRefGoogle Scholar
  32. Davis LA, Gordon T, Hoffer JA, Jhamandas J & Stein RB (1978). Compound action potentials recorded from mammalian peripheral nerves following ligation and resuturing. Journal of Physiology (London) 285, 543–559.Google Scholar
  33. Denny-Brown, D (1929). On the nature of postural reflexes. Proceedings of Royal Society (Biology) 104, 252–301.CrossRefGoogle Scholar
  34. Dhoot GK & Vrbova G (1991). Conversion of cat and rabbit soleus muscle fibres by alien nerves. Muscle & Motility 2, 125–130.Google Scholar
  35. Donselaar Y, Eerbeek O, Kernell D & Verhey BA (1987). Fibre sizes and histochemical staining characteristics in normal and chronically stimulated fast muscle of cat. Journal of Physiology (London) 382, 237–254.Google Scholar
  36. Dubois DC & Almon RR (1980). Disuse atrophy of skeletal muscle is associated with an increase in number of glucocorticoid receptors. Endocrinology 107: 1649–1651.PubMedCrossRefGoogle Scholar
  37. Dum RP, O’Donovan MJ, Toop J, Tsairis P, Pinter MJ & Burke RE (1985). Cross-reinnervated motor units in cat muscle. II. Soleus muscle reinnervated by flexor digitorum longus motoneurons. Journal of Neurophysiology 54, 837–851.PubMedGoogle Scholar
  38. Edstrom L & Grimby L (1986). Effect of exercise on the motor unit. Muscle & Nerve 9, 104–126.CrossRefGoogle Scholar
  39. Eerbeek O, Kernell D & Verhey BA (1984). Effects of fast and slow patterns of tonic long-term stimulation on contractile properties of fast muscles in cat. Journal of Physiology (London) 352, 73–90.Google Scholar
  40. Eisenberg BR & Salmons S (1981). The reorganization of subcellular structure in muscle undergoing fast-to-slow type transformation. A streological study. Cell Tissue Research 220, 449–471.PubMedCrossRefGoogle Scholar
  41. Enoka RM (1988). Muscle strength and its development: new perspectives. Sports Medicine 6, 148–168.CrossRefGoogle Scholar
  42. Fenn WO (1923). A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. Journal of Physiology (London) 58, 175–203.Google Scholar
  43. Fitts RH, Metzger DA, Riley DA & Unsworth BR (1986). Models of disuse: a comparison of hindlimb suspension and immobilization. Journal of Applied Physiology 60, 1946–1953.PubMedCrossRefGoogle Scholar
  44. Fournier M, Roy RR, Perham H, Simard CP & Edgerton VR (1983). Is immobilisation a model of disuse? Experimental Neurology 80, 147–156.PubMedCrossRefGoogle Scholar
  45. Fox EL, Bowers RW & Foss ML (1988). The Physiological Basis of Physical Education and Athletics. New York: WB Saunders.Google Scholar
  46. Fox EL, Bowers RW & Foss ML (1993). The Physiological Basis for Exercise and Sport, 5th Ed. Dubuque, IA: Wm. C. Brown Communications, Inc.Google Scholar
  47. Frischknecht R & Vrbova G (1991). Adaptation of rat extensor digitorum longus to overload and increased activity. Pflügers Archiv 419, 319–326.PubMedCrossRefGoogle Scholar
  48. Fu S, Gordon T, Parry DJ & Tyreman N (1992). Immunohistochemical analysis of fiber types within physiologically typed motor units of rat tibialis anterior muscle after long-term cross-reinnervation. Society for Neuroscience Abstracts 18, 1557.Google Scholar
  49. Gardiner PG (1991). Effects of exercise training on components of the motorunit. Canadian Journal of Sports Sciences 16, 271–288.Google Scholar
  50. Gardiner PG, Favron M & Corriveau P (1992). Histochemical and contractile responses of rat medial gastrocnemius to two weeks of complete disuse. Canadian Journal of Physiology and Pharmacology 70, 1075–81.PubMedCrossRefGoogle Scholar
  51. Gardiner PG, Montanaro DS & Edgerton VR (1980). Effects of glucocortocoid treatment and food restriction on rat hindlimb muscles. Pflügers Archiv 385, 147–153.PubMedCrossRefGoogle Scholar
  52. Gauthier GF, Burke RE, Lowey S & Hobbs AW (1983). Myosin isozymes in normal and cross-reinnervated cat skeletal muscle fibers. Journal of Cell Biology 97, 756–771.PubMedCrossRefGoogle Scholar
  53. Gillespie MJ, Gordon T & Murphy PA (1986). Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve. Journal of Physiology (London) 372, 485–500.Google Scholar
  54. Gillespie MJ, Gordon T & Murphy PA (1987). Motor units and histochemistry in the rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation. Journal of Neurophysiology 57, 921–937.PubMedGoogle Scholar
  55. Gimbrone MA (1984). Macrophages, neovascularisation and the growth of vascular cells. In: Jaffe EA (ed), Biology of Endothelial Cells, pp. 97–107. Boston: Martinus Nihoff Publications.CrossRefGoogle Scholar
  56. Goldspink G, Scutt A, Loughna PT, Wells DJ, Jaenicke T & Gerlach GF (1992). Gene expression in skeletal muscle in response to stretch and force generation. American Journal of Physiology 262, R356–R363.PubMedGoogle Scholar
  57. Gollnick PD, Armstrong RB, Saltin B, Saubert CW, Sembrowich WL & Shepherd RE (1973). Effect of training on enzyme activity and fiber composition of human skeletal muscle. Journal of Applied Physiology 34, 107–111.PubMedGoogle Scholar
  58. Gollnick PD, Armstrong RB, Saubert IV CW, Piehl K & Saltin B (1972). Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. Journal of Applied Physiology 33, 312–319.PubMedGoogle Scholar
  59. Gollnick PD, Piehl K & Saltin B (1974). Selective glycogen depletion pattern in human skeletal muscle fibres after exercise of varying intensity and at varying pedaling rates. Journal of Physiology (London) 216, 1502–1509.Google Scholar
  60. Gollnick PD, Timson BF, Moore RL & Riedy M (1981). Muscular enlargement and the number of fibers in the skeletal muscles of rats. Journal of Applied Physiology: Respiratory Environment Exercise Physiology 50, 936–943.Google Scholar
  61. Gordon T (1987). Muscle plasticity as demonstrated during sprouting and reinnervation. American Zoology 27, 1055–1066.Google Scholar
  62. Gordon T & Mao J (1994). Muscle atrophy and procedures for training for spinal cord injury. Physical Therapy 74, 50–60.PubMedGoogle Scholar
  63. Gordon T & Pattullo MC (1993). Plasticity of muscle fiber and motor unit types. Exercise and Sports Sciences Reviews 21, 331–362.Google Scholar
  64. Gordon T, Thomas CK, Stein RB & Erdebil S (1988). Comparison of physiological and histochemical properties of motor units after cross-reinnervation of antagonistic muscles in the cat hindlimb. Journal of Neurophysiology 60, 365–378.PubMedGoogle Scholar
  65. Gorza L, Gundersen K, Lomo T, Schiaffino S & Westgaard, RH (1988). Slow-to-fast transformation of denervated soleus muscles by chronic high-frequency stimulation in the rat. Journal of Physiology (London) 402, 627–749.Google Scholar
  66. Green HJ, Dusterhoft S, Dux L & Pette D (1992). Metabolite patterns related to exhaustion, recovery, and transformation of chronically stimulated rabbit fast-twitch muscle. Pflügers Archiv 420, 359–366.PubMedCrossRefGoogle Scholar
  67. Green HJ, Klug GA, Reichman H, Seedorf U, Wiehrer W & Pette D (1984). Exercise-induced fibre type transitions with regard to myosin, parvalbumin, and sarcoplasmic reticulum in muscles of the rat. Pflügers Archiv 400, 432–438.PubMedCrossRefGoogle Scholar
  68. Graham SC, Roy RR, Navarro B, Jaing B, Pierotti D, Bodine-Fowler S & Edgerton VR (1992). Enzyme and size profiles n chronically inactive cat soleus muscle fibers. Muscle & Nerve 15, 27–36.CrossRefGoogle Scholar
  69. Grounds MD (1991). Towards understanding skeletal muscle regeneration. Pathology Research Practice 187, 1–22.CrossRefGoogle Scholar
  70. Gundersen K, Leberer E, Lömo T, Pette D & Staron RS (1988). Fibre types, calcium-sequestering proteins and metabolic enzymes in denervated and chronically stimulated muscles of the rat. Journal of Physiology (London) 398, 177–189.Google Scholar
  71. Gutmann E, Schiaffino S & Hanzlikova V (1971). Mechanism of compensatory hypertrophy in skeletal muscle of the rat. Experimental Neurology 31, 451–464.PubMedCrossRefGoogle Scholar
  72. Hagerman FC (1992). Energy metabolism and fuel utilization. Medical Sciences Sports Exercise 24, S309–S314.Google Scholar
  73. Hartner K-T, Kirschbaum BJ & Pette D (1989). The multiplicity of troponin T isoforms. Normal rabbit muscles and effects of chronic stimulation. European Journal of Biochemistry 179, 31–38.PubMedCrossRefGoogle Scholar
  74. Henneman E & Mendell LM (1981). Functional organization of the motoneurone pool and its inputs. In: Brookhart JM, Mountcastle VB (sec. eds.), Brooks VB (vol. ed.), Handbook of Physiology, sec. 1. vol. II, pt. 1, The Nervous System: Motor Control, pp. 423-508, Bethesda: Ameriocan Physiological Society.Google Scholar
  75. Henriksson J (1992). Effects of physical training on the metabolism of skeletal muscle. Diabetes Care 15, 1701–1711.PubMedCrossRefGoogle Scholar
  76. Henriksson J, Chi MM-Y, Hintz CS, Young DA, Salmons S & Lowry OH (1986). Chronic stimulation of mammalian muscle: changes in enzymes of six metabolic pathways. American Journal of Physiology 251, C614–C632.PubMedGoogle Scholar
  77. Herbert ME, Roy RR & Edgerton VR (1988). Influence of one-week hindlimb suspension and intermittent high load exercise on rat muscles. Experimental Neurology 102, 190–198.PubMedCrossRefGoogle Scholar
  78. Hicks A & McComas AJ (1989). Increased sodium pump activity following repetitive stimulation of rat soleus muscles. Journal of Physiology (London) 414, 337–349.Google Scholar
  79. Hnik P, Vejsada R, Goldspink DF, Kasicki S & Krekule I (1985). Quantitative evaluation of electromyogram activity in rat extensor and flexor muscles immobilized at different lengths. Experimental Neurology 88, 515–528.PubMedCrossRefGoogle Scholar
  80. Hoffmann SJ, Roy RR, Bianco CE & Edgerton VR (1990). Enzyme profiles of single muscle fibers in the absence of normal neuromuscular activity. Journal of Applied Physiology 69, 1150–1158.PubMedGoogle Scholar
  81. Holloszy JO & Booth FW (1976). Biochemical adaptations to endurance exercise in muscle. Annual Reviews of Physiology 38, 273–291.CrossRefGoogle Scholar
  82. Hood DA, Zak R & Pette D (1989). Chronic stimulation of rat skeletal muscle induces coordinate increases in mitochondrial and nuclear mRNAs of cytochrome c oxidase subunits. European Journal of Biochemistry 179, 275–280.PubMedCrossRefGoogle Scholar
  83. Hoppeler H (1988). Exercise-induced structural changes of skeletal muscle. ISI Atlas Science Biochemistry 1, 247–255.Google Scholar
  84. Hudlicka O (1984). Development of microcirculation: capillary growth and adaptation. In: Renkin EM, Michel CC, Geiger SR (eds), Handbook of Physiology, sec. 2, The Cardiovascular System, pp 165–216. Baltimore, MD: Williams and Wilkins.Google Scholar
  85. Hudlicka O, Brown M, Cotter M, Smith M & Vrbova G (1977). The effect of long-term stimulation of fast muscles on their blood flow, metabolism and ability to withstand fatigue. Pflügers Archiv 369, 141–149.PubMedCrossRefGoogle Scholar
  86. Hudlicka O, Tyler KR, Srihari T, Heilig A & Pette D (1982). The effect of different patterns of long-term stimulation on contractile properties and myosin light chains in rabbit fast muscles. Pflügers Archiv 393, 164–170.PubMedCrossRefGoogle Scholar
  87. Humphreys PW & Lind AR (1963). The blood flow through active and inactive muscles of the forearm during sustained hand-grip contractions. Journal of Physiology (London) 166, 12–131.Google Scholar
  88. Jablecki CK, Heuser JE & Kaufman S (1973). Auto-radiographic localisation of new RNA synthesis in hypertrophying skeletal muscle. Journal of Cellular Biology 57, 743–759.CrossRefGoogle Scholar
  89. James NT (1976). Compensatory hypertrophy in the extensor digitorum longus muscle of the mouse. Journal of Anatomy 122, 121–131.PubMedGoogle Scholar
  90. Jansson E & Kaijser L (1977). Muscle adaptation to extreme endurance training in man. Acta Physiology Scandinavica 100, 315–325.CrossRefGoogle Scholar
  91. Jiang B, Ohira Y, Roy RR, Nguyen Q, Ilyina-Kakueva EI, Oganov V & Edgerton VR (1992). Adaptation of fibers in fast-twitch muscles of rats to spaceflight and hindlimb suspension. Journal of Applied Physiology Supplement 73, 58S–65S.Google Scholar
  92. Jiang B, Roy RR & Edgerton VR (1990a). Expression of a fast fiber enzyme profile in the cat soleus after spinalization. Muscle & Nerve 13, 1037–1049.CrossRefGoogle Scholar
  93. Jiang B, Roy RR & Edgerton VR (1990b). Enzymatic plasticity of medial gastrocnemius fibers in the adult chronic spinal cat. American Journal of Physiology 259, C507–C514.PubMedGoogle Scholar
  94. Jiang B, Roy RR, Navarro C, Nguyen Q, Pierotti D & Edgerton VR (1991). Enzymatic responses of cat medial gastrocnemius fibers to chronic inactivity. Journal of Applied Physiology 70, 231–239.PubMedGoogle Scholar
  95. Jones DA, Rutherford OM & Parker DF (1989). Physiological changes in skeletal muscle as a result of strength training. Quarterly Journal Experimental Physiology 74, 233–256.Google Scholar
  96. Kernell D, Donselaar Y & Eerbeek O (1987b). Effects of physiological amounts of high-and low-rate chronic stimulation on fast-twitch muscle of the cat hindlimb. 11. Endurance-related properties. Journal of Neurophysiology 58, 614–627.PubMedGoogle Scholar
  97. Kernell D & Eerbeek O (1989). Physiological effects of different patterns of chronic stimulation on muscle properties. In: Rose FC, Jones R (eds), Neuromuscular Stimulation, pp 193–200. New York: Demos.Google Scholar
  98. Kernell D, Eerbeek O, Verhey BA & Donselaar Y (1987a). Effects of physiological amounts of high-and low-rate chronic stimulation on fast-twitch muscle of the cat hindlimb. I. Speed and force-related properties. Journal of Neurophysiology 58, 598–613.PubMedGoogle Scholar
  99. Klagsbrun M (1989). The fibroblast growth factor family: structural and biological properties. Progress in Growth Factor Research 1, 207–235.PubMedCrossRefGoogle Scholar
  100. Komi PV, Viitasalo JHT, Havu M, Thorstensson A, Sjodin B & Karsson J (1977). Skeletal muscle fibres and muscle enzyme activities in monozygous and dizygous twins of both sexes. Acta Physiology Scandinavica 100, 385–392.Google Scholar
  101. Knighton DR, Hunt TK, Scheunesnstuhl H, Halliday BJ, Werb Z & Banda MJ (1983). Oxygen tension regulates the expression of angiogenic factor by macrophages. Science 221, 1283–1285.PubMedCrossRefGoogle Scholar
  102. Krieger DA, Tate CA, McMillin-Wood J & Booth FW (1980). Populations of rat skeletal muscle mitochondria after exercise and immobilization. Journal of Applied Physiology 48, 23–28.PubMedGoogle Scholar
  103. Kuffler SW & Vaughn-Williams EM (1953). Properties of the “slow” skeletal muscle fibres of the frog. Journal of Physiology (London) 121, 318–340.Google Scholar
  104. Kugelberg E, Edstrom L & Abruzzese M (1970). Mapping of motor units in experimentally reinnervated rat muscle. Journal of Neurology, Neurosurgery and Psychiatry 33, 310–329.CrossRefGoogle Scholar
  105. Kugelberg E & Lindegren B (1979). Transmission and contraction fatigue of rat motor units in relation to succinate dehydrogenase activity of motor unit fibres. Journal of Physiology (London) 288, 285–300.Google Scholar
  106. Kühne W (1863). Uber die Endignung der Nerven in den Muskeln. Vischow Archives 27, 508–533.CrossRefGoogle Scholar
  107. Lamb DR, Peter JB, Jeffress RN & Wallace HA (1969). Glycogen, hexokinase, and glycogen synthetase adaptations to exercise. American Journal of Physiology 217, 1628–1632.PubMedGoogle Scholar
  108. Lamb GD & Stephenson DG (1991). Effect of Mg2+ on the control of Ca2+ release in skeletal muscle fibres of the toad. Journal of Physiology (London) 434, 507–528.Google Scholar
  109. Leberer E, Hartner K-T, Brandi CJ, Fujii J, Tada M, MacLennan DH & Pette D (1989). Slow\cardiac sarcoplasmic reticulum Ca-ATPase and phospholamban mRNAs are expressed in chronically stimulated rabbit fast-twitch muscle. European Journal of Biochemistry 185, 51–54.PubMedCrossRefGoogle Scholar
  110. Leberer E, Hartner K-T & Pette D (1987). Reversible inhibition of sarcoplasmic reticulum Ca-ATPase by altered neuromuscular activity in rabbit fast-twitch muscle. European Journal of Biochemistry 62, 255–561.Google Scholar
  111. Leberer E, Seedorf U & Pette D (1986). Neural control of gene expression in skeletal muscle Ca-sequestering proteins in developing and chronically stimulated rabbit skeletal muscles. Biochemical Journal 239, 295–300.PubMedGoogle Scholar
  112. Lieber RL, Friden JO, Hargens, AR, Danzig LA & Gershuni DH (1988). Differential response of the dog quadriceps muscle to external skeletal fixation of the knee. Muscle & Nerve 11, 193–201.CrossRefGoogle Scholar
  113. Longhurst JC, Kelly AR, Gonyea WJ & Mitchell JH (1980a). Echocardiographic left ventricular mass in distance runners and weight lifters. Journal of Applied Physiology 48, 154–162.PubMedGoogle Scholar
  114. Longhurst JC, Kelly AR, Gonyea WJ & Mitchell JH (1980b). Cardiovascular responses to static exercise in distance runners and weight lifters. Journal of Applied Physiology 49, 676–683.PubMedGoogle Scholar
  115. Longhurst JC & Mitchell JH (1983). Does endurance training benefit the cardiovascular system? Journal of Cardiovascular Medicine 8, 227–236.Google Scholar
  116. Longhurst JC & Stebbins CL (1992). The isometric athlete. Cardiology Clinics 10, 281–294.PubMedGoogle Scholar
  117. Lovely RG, Gregor RJ, Roy RR & Edgerton VR (1990). Weight-bearing hindlimb stepping in treadmill exercised adult spinal cats. Brain Research 514, 206–218.PubMedCrossRefGoogle Scholar
  118. MacDougall JD, Sale DG, Elder DG, Elder GB & Sutton JR (1982). Muscle ultrastructural characteristics of elite power lifters and bodybuilders. European Journal of Applied Physiology 48, 117–126.CrossRefGoogle Scholar
  119. MacDougall JD, Ward GR, Sale DG & Sutton JR (1977). Biochemical adaptation of human skeletal muscle to heavy resistance training and immobilization. Journal of Applied Physiology: Respiratory Environment Exercise Physiology 43, 700–703.Google Scholar
  120. Margreth A, Salviati G & Carraro U (1973). Neural control of the activity of the calcium transport system in sarcoplasmic reticulum of rat skeletal muscle. Nature 241, 285–286.PubMedCrossRefGoogle Scholar
  121. Mayer RF, Burke RE, Toop J, Hodgson JA, Kanda K & Walmsley B (1981). The effect of long-term immobilization on the motor unit population of the cat medial gastrocnemius muscle. Neuroscience 6, 725–739.PubMedCrossRefGoogle Scholar
  122. Mayer RF, Burke RE, Toop J, Walmsley & Hodgson JA (1984). The effect of spinal cord transection on motor units in cat medial gastrocnemius muscles. Muscle & Nerve 7, 23–31.CrossRefGoogle Scholar
  123. McMinn RMH & Vrbova G (1964). The effect of tenotomy on the structure of fast and slow muscle in the rabbit. Quarterly Journal of Experimental Physiology 49, 424–429.Google Scholar
  124. McMinn RMH & Vrbova G (1967). Motoneurone activity as a cause of degeneration in the soleus muscle of the rabbit. Quarterly Journal of Experimental Physiology 52, 411–415, 1967.Google Scholar
  125. Mero A, Komi PV & Gregor RJ (1992). Biomechanics of sprint running. A review. Sports Medicine 13, 376–392.PubMedCrossRefGoogle Scholar
  126. Mero A, Luhtanen P, Viitasalo JT & Komi PV (1981). Relationships between the maximal running velocity, muscle fiber characteristics, force production and force relaxation of sprinters. Scandinavian Journal of Sports Sciences 3, 16–22.Google Scholar
  127. Morgan TE, Short FA & Cobb LA (1969). Effect of long-term exercise on skeletal muscle lipid composition. American Journal of Physiology 216, 82–86.PubMedGoogle Scholar
  128. Munson JB, Foerhing RC, Loften SA, Zengel JE & Sypert GW (1986) Plasticity of medial gastrocnemius motor units following cordotomy in the cat. Journal of Neurophysiology 55, 619–634.PubMedGoogle Scholar
  129. Nagesser AS, van der Laarse WJ & Elzinga G (1992). Metabolic changes with fatigue in different types of single muscle fibres of Xenopus Laevis. Journal of Physiology (London) 448, 511–523.Google Scholar
  130. Narici MV, Roi GS, Landoni L, Minetti AE & Cerretelli P (1989). Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. European Journal of Applied Physiology 59, 310–319.CrossRefGoogle Scholar
  131. Nemeth PM, Solanki L, Gordon DA, Hamm TM, Reinking RM & Stuart DG (1986). Uniformity of metabolic enzymes within individual motor units. Journal of Neuroscience 6, 892–898.PubMedGoogle Scholar
  132. Nguyen PV & Atwood HL (1994). Altered impulse activity modifies synaptic physiology and mitochondrial rhodamine-123 florescence in crayfish phasic motor neurons. Journal of Neurophysiology 72, 2944–2955.PubMedGoogle Scholar
  133. Ohira Y, Jiang B, Roy RR, Oganov V, Ilyina-Kakueva E, Marini JF & Edgerton VR (1992). Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. Journal of Applied Physiology Supplement 73, 51S–57S.Google Scholar
  134. Ohlendieck K, Briggs KN, Lee KF, Wechsler AW & Campbell KP (1991). Analysis of excitation-contraction-coupling components in chronically stimulated canine skeletal muscle. European Journal of Biochemistry 02, 739–747.CrossRefGoogle Scholar
  135. Olha AE, Jasmin BJ, Michel RN & Gardiner PF (1988). Physiological responses of rat plantaris motor units to overload induced by surgical removal of its synergists. Journal of Neurophysiology 60, 2138–2151.PubMedGoogle Scholar
  136. Peter JB, Barnard RJ, Edgerton VR, Gillespie CA & Stempel KE (1972). Metabolic profiles of three fibre types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11, 2627–2633.PubMedCrossRefGoogle Scholar
  137. Pette D & Hofer HW (1980). The constant proportion enzyme group concept in the selection of reference enzymes in metabolism. Trends in Enzyme Histochemistry and Cytochemistry: Excerpta Medica (Ciba Foundation Symposium) 73, 231–244.Google Scholar
  138. Pette D & Luh W (1962). Constant-proportion groups of multilocated enzymes. Biochemistry Biophysics Research Communications 8, 283–287.CrossRefGoogle Scholar
  139. Pette D, Muller W, Leisner E & Vrbova G (1976). Time dependent effects on contractile properties, fibre population, myosin light chains and enzymes of energy metabolism in intermittently and continuously stimulated fast twitch muscle of the rabbit. Pflügers Archiv 364, 103–112.PubMedCrossRefGoogle Scholar
  140. Pette D, Smith ME, Staudte HW & Vrbova G (1973). Effects of long-term electrical stimulation on some contractile and metabolic characteristics of fast rabbit muscles. Pflügers Archiv 338, 257–272.PubMedCrossRefGoogle Scholar
  141. Pette D & Staron RS (1990). Cellular and molecular diversities of mammalian skeletal muscle fibres. Reviews of Physiology, Biochemistry and Pharmacology 116, 1–76.PubMedGoogle Scholar
  142. Pette D & Vrbová G (1992). Adaptation of mammalian skeletal muscle to chronic electrical stimulation. Reviews of Physiology, Biochemistry and Pharmacology 120, 115–202.PubMedCrossRefGoogle Scholar
  143. Pierotti DJ, Roy RR, Bodine-Fowler SC, Hodgson JA & Edgerton VR (1991). Mechanical and morphological properties of chronically inactive cat tibialis anterior motor units. Journal of Physiology (London) 444, 175–192.Google Scholar
  144. Pierotti DJ, Roy RR, Flores V & Edgerton VR (1990). Influence of 7 days of hindlimb suspension and intermittent weight support on rat muscle mechanical properties. Aviation Space Environmental Medicine 61, 205–210.Google Scholar
  145. Ranvier L (1874). De quelques faits relatifs á l’histologie et á la physiologie des muscles stries. Archives Physiology and Normal Pathology 6, 1–15.Google Scholar
  146. Reid CM, Yeater RA & Ullrich H (1987). Weight training and strength, cardiorespiratory functioning and body composition of men. British Journal of Sports Medicine 21, 40–44.PubMedCrossRefGoogle Scholar
  147. Riedy MR, Moore RL & Gollnick PD (1985). Adaptive response of hypertrophied skeletal muscle to endurance training. Journal of Applied Physiology 59, 127–131.PubMedGoogle Scholar
  148. Rifenberick DH, Gamble J & Max SR (1973). Response of mitochondrial enzymes to decreased muscular activity. American Journal of Physiology 225, 1295–1299.PubMedGoogle Scholar
  149. Rosenblatt JD & Parry DJ (1993). Adaptation of rat extensor digitorum longus muscle to gamma irradiation and overload. Pflügers Archiv 423, 255–264.PubMedCrossRefGoogle Scholar
  150. Roy RR & Acosta L Jr (1986). Fiber type and fiber size changes in selected thigh muscles six months after low thoracic spinal cord transection in adult cats: Exercise effects. Experimental Neurology 92, 675–685.PubMedCrossRefGoogle Scholar
  151. Roy RR, Baldwin KM & Edgerton VR (1991). The plasticity of skeletal muscle: effects of neuromuscular activity. Exercise Sports Sciences Reviews 19, 269–312.Google Scholar
  152. Roy RR, Bello MA, Bouissou P & Edgerton VR (1987). Size and metabolic properties of fibers in rat fast-twitch muscles after hindlimb suspension. Journal of Applied Physiology 62, 2348–2357.PubMedGoogle Scholar
  153. Roy RR, Hodgson JA, Chalmers GR, Buxton W & Edgerton VR (1992). Responsiveness of the cat plantaris to functional overload. In: Sato Y, Portmans J, Hashimoto I, Oshida Y (eds), Integration of Medical and Sports Sciences, Medical Sport Sciences 37, pp. 43-51. Basel: Karger.Google Scholar
  154. Roy RK, Mabuchi K, Sarkar S, Mis C & Sreter FA (1979). Changes in tropomyosin subunit pattern in chronic electrically stimulated rabbit fast muscles. Biochemistry Biophysics Research Communications 89, 181–187.CrossRefGoogle Scholar
  155. Russell B, Dix DJ, Haller DL & Jacobs-El J (1992). Repair of injured skeletal muscle: A molecular approach. Medicine and Science in Sports and Exercise 24, 189–196.PubMedCrossRefGoogle Scholar
  156. Sahlin K (1978). Intracellular pH and energy metabolism in skeletal muscle in man. Acta Physiology Scandinavica Supplement 455 1–56.Google Scholar
  157. Salmons S & Henriksson J (1986). The adaptive response of skeletal muscle to increased use. Muscle & Nerve 4, 94–105.CrossRefGoogle Scholar
  158. Salmons S & Sreter FA (1976). Significance of impulse activity in the transformation of skeletal muscle type. Nature 263, 30–34.PubMedCrossRefGoogle Scholar
  159. Salmons S & Vrbova G (1969). The influence of activity on some contractile characteristics of mammalian fast and slow muscles. Journal of Physiology (London) 201, 535–549.Google Scholar
  160. Saltin B & Gollnick PD (1983). Skeletal muscle adaptability: significance for metabolism and performance. In: Geiger SR, Adrian RH (eds.), Peachey LD (sec. ed.), Handbook of Physiology, sec. 10, Skeletal Muscle. Specialization, Adaptation, and Disease, pp. 555-631. Bethesda, MD: American Physiological Society.Google Scholar
  161. Saubert CW, Armstrong IV RB, Shepherd RE & Gollnick PD (1973). Anaerobic enzyme adaptations to sprint training in rats. Pflügers Archiv 341, 305–312.PubMedCrossRefGoogle Scholar
  162. Schantz PG, Henriksson J & Jansson E (1983). Adaptation of human skeletal muscle to endurance training of long duration. Clinical Physiology 3, 141–151.PubMedCrossRefGoogle Scholar
  163. Schiaffino S & Bormioli SP (1973). Adaptive changes in developing rat skeletal muscle in response to functional overload. Experimental Neurology 40, 126–137.PubMedCrossRefGoogle Scholar
  164. Schmalbruch H & Hellhamer U (1977). The nuclei in adult rat muscles with special reference to satellite cells. Anatomical Records 189, 169–176.CrossRefGoogle Scholar
  165. Schulte LM, Navarro J & Kandarian SC (1993). Regulation of sarcoplasmic reticulum calcium pump gene expression by hindlimb unweighting. American Journal of Physiology 264 (Cellular Physiology 33), C1308–C1315.PubMedGoogle Scholar
  166. Sesodia S, Gordon T & Nemeth P (1993). Increased metabolic enzyme heterogeneity of muscle unit fibers after reinnervation. Society for Neuroscience Abstracts 19, 152.Google Scholar
  167. Sjøgaard G (1987). Muscle fatigue. Medical Sport Sciences 26, 98–109.Google Scholar
  168. Smith JS, Coronado R & Meissner G (1985). Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels. Nature 316, 736–738.CrossRefGoogle Scholar
  169. Spector SA (1985a). Effects of elimination of activity on contractile and histochemical properties of rat soleus muscle. Journal of Neuroscience 5, 2177–2188.PubMedGoogle Scholar
  170. Spector SA (1985b). Trophic effects on the contractile and histochemical properties of rat soleus muscle. Journal of Neuroscience 5, 2189–2196.PubMedGoogle Scholar
  171. Sreter FA, Gergely J, Salmons S & Romanul F (1973). Synthesis by fast muscle of myosin light chains characteristic of slow muscle in response to long term stimulation. Nature New Biology 241, 17–19.Google Scholar
  172. Sreter FA, Lopez JR, Alamo L, Mabuchi K & Gergely J (1987). Changes in intracellular ionized Ca concentration associated with muscle fiber type transformation. American Journal of Physiology 253, C296–300.PubMedGoogle Scholar
  173. Sreter FA, Luff AR & Gergely J (1976). Effect of cross-reinnervation on physiological parameters and on properties of myosin and sarcoplasmic reticulum of fast and slow muscles of the rabbit. Journal of General Physiology 66, 811–821.CrossRefGoogle Scholar
  174. Sreter FA, Pinter K, Jolesz F & Mabuchi K (1982). Fast to slow transformation of fast muscles in response to long-term phasic stimulation. Experimental Neurology 75, 95–102.PubMedCrossRefGoogle Scholar
  175. Stein RB, Gordon T, Jefferson J, Sharfenberger A, Yang JE, Totosy de Zepetnek & Belanger M (1992). Optimum stimulation of paralysed muscle in spinal cord patients. Journal of Applied Physiology 72, 1393–1400.PubMedGoogle Scholar
  176. St-Pierre D & Gardiner P (1985). Effect of “disuse” on mammalian fast-twitch muscle: joint fixation compared to neurally applied tetrodotoxin. Experimental Neurology 90, 635–651.PubMedCrossRefGoogle Scholar
  177. Sweeney HL, Kushmerick MJ, Mabuchi K, Sreter FA & Gergely J (1988). Myosin light chain and heavy chain variations correlate with altered shortening velocity of isolated skeletal muscle fibers. Journal of Biological Chemistry 263, 9034–9039.PubMedGoogle Scholar
  178. Tabary JC, Tabary C, Tardieu C, Tardieu G & Goldspink G (1972). Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts. Journal of Physiology (London) 224, 231–244.Google Scholar
  179. Taylor AW, Thayer R & Rao S (1972). Human skeletal muscle glycogen synthase activities with exercise and training. Canadian Journal of Physiology and Pharmacology 52, 119–122.CrossRefGoogle Scholar
  180. Templeton G, Padalino M, Manton J, Leconey T, Hagler H & Glasberg M (1984). The influence of rat suspension-hypokinesia on the gastrocnemius muscle. Aviation Space Environmental Medicine 55, 381–386.Google Scholar
  181. Templeton GH, Sweeney HL, Timson BF, Padalino M & Dudenhoeffer GA (1988). Changes in fiber composition of soleus muscle during hindlimb suspension. Journal of Applied Physiology 65, 1191–1195.PubMedGoogle Scholar
  182. Terjung RL (1976). Muscle fiber involvement during training of different intensities and durations. American Journal of Physiology 230, 946–950.PubMedGoogle Scholar
  183. Thomason DB & Booth FW (1990). Atrophy of the soleus muscle by hindlimb unweighting. Journal of Applied Physiology 68, 1–12.PubMedCrossRefGoogle Scholar
  184. Thompson JA, Anderson KD, Di Pietro JM, Swiebel JA, Zametta M, Anderson WF & Maciag T (1988) Site-directed neovessel formation in vivo. Science 241, 1349–1352.PubMedCrossRefGoogle Scholar
  185. Totosy de Zepetnek J, Zung HV, Erdebil S & Gordon T (1992a). Innervation ratio is an important determinant of force in normal and reinnervated rat tibialis anterior muscle. Journal of Neurophysiology 67, 1385–1403.PubMedGoogle Scholar
  186. Totosy de Zepetnek JE, Zung HV, Erdebil S & Gordon T (1992b). Motor unit categorization on the basis of contractile and histochemical properties: a glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle. Journal of Neurophysiology 67, 1404–1415.PubMedGoogle Scholar
  187. Trivedi B & Danforth WH (1966). effect of pH on the kinetics of frog muscle phosphofructokinase. Journal of Biological Chemistry 241, 4110–4112.PubMedGoogle Scholar
  188. Tsika RW, Herrick RE & Baldwin KM (1987). Time course of adaptation in rat skeletal muscle isomyosin during compensatory growth and regression. Journal of Applied Physiology 63, 2111–2121.PubMedGoogle Scholar
  189. Vrbova G (1963). The effect of motoneurone activity on the speed of contraction of striated muscle. Journal of Physiology (London) 169, 513–526.Google Scholar
  190. Vrbova G, Gordon T & Jones R (1994). Nerve-Muscle Interaction. London: Chapman & Hall.Google Scholar
  191. Walsh JV, Burke RE, Rymer WZ & Tsairis P (1978). Effect of compensatory hypertrophy studied in individual motor units in medial gastrocnemius muscle of the cat. Journal of Neurophysiology 41, 496–508.PubMedGoogle Scholar
  192. Westerblad H, Lee JA, Lannergren J & Allen DG (1991). Cellular mechanisms of fatigue in skeletal muscle. American Journal of Physiology 261, C195–C209.PubMedGoogle Scholar
  193. Williams RS, Garcia-Moll M, Mellor J, Salmons S & Harlan W (1987). Adaptation of skeletal muscle to increased contractile activity. Expression of nuclear genes encoding mitochondrial proteins. Journal of Biological Chemistry 262, 2764–2767.PubMedGoogle Scholar
  194. Williams RS, Salmons S, Newsholme EA, Kaufman RE & Mellor J (1986). Regulation of nuclear and mitochondrial gene expression by contractile activity in skeletal muscle. Journal of Biological Chemistry 261, 376–380.PubMedGoogle Scholar
  195. Winiarski AM, Roy RR, Alford EK, Chiang PC & Edgerton VR (1987). Mechanical properties of rat skeletal muscle after hind limb suspension. Experimental Neurology 96, 650–660.PubMedCrossRefGoogle Scholar
  196. Witzmann FA, Kim DH & Fitts RH (1983). Effect of hindlimb immobilization on the fatigability of skeletal muscle. Journal of Applied Physiology 54, 1242–1248.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • T. Gordon
    • 1
  1. 1.Department of Pharmacology, Division of NeurosciencesUniversity of AlbertaEdmontonCanada

Personalised recommendations