Fatigue pp 241-258 | Cite as

Overview: Potential Role of Segmental Motor Circuitry in Muscle Fatigue

  • U. Windhorst
  • G. Boorman
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 384)


This chapter reviews several mechanisms that the CNS may use to mitigate muscle fatigue, including intrinsic motoneuron properties and feedback systems. The emphasis is on the effects of sensory inputs on spinal cord interneurons including: Renshaw cells; Ib inhibitory interneurons; interneurons mediating presynaptic inhibition; Ia inhibitory interneurons; and interneuronal networks constituting central pattern generators for locomotion. This exercise brings out how little is known about the operation of these circuits in dealing with muscle fatigue.


Motor Unit Muscle Fatigue Central Pattern Generator Presynaptic Inhibition Muscle Afferents 
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  1. Baldissera F, Hultborn H & Illert M (1981). Integration in spinal neuronal systems. In: Brooks VB (ed.), Handbook of Physiology, Vol. II, Part 1, The Nervous System, pp. 509–595. Bethesda: American Physiological Society.Google Scholar
  2. Bevan L, Laouris Y, Reinking RM & Stuart DG (1992). The effect of the stimulation pattern on the fatigue of single motor units in adult cats. Journal of Physiology (London) 449, 85–108.Google Scholar
  3. Bigland-Ritchie BR (1993). Regulation of motorneuron firing rates in fatigue. In: Sargeant AJ, Kernell D (eds.), Neuromuscular Fatigue, pp 147-155. Amsterdam: Royal Netherlands Academy of Arts and Sciences.Google Scholar
  4. Bigland-Ritchie B, Dawson NJ, Johansson RS & Lippold OCJ (1986). Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. Journal of Physiology (London) 379, 451–459.Google Scholar
  5. Bigland-Ritchie B, Johansson RS, Lippold OCJ & Woods JJ (1983a). Changes in motoneurone firing rates during sustained maximal voluntary contractions. Journal of Physiology (London) 340, 335–346.Google Scholar
  6. Bigland-Ritchie B, Johansson RS, Lippold OCJ & Woods JJ (1983b). Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. Journal of Neurophysiology 50, 313–324.PubMedGoogle Scholar
  7. Bigland-Ritchie B & Woods JJ (1984). Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle & Nerve 7, 691–699.CrossRefGoogle Scholar
  8. Binder MD & Mendell LM (eds.) (1990). The Segmental Motor System. New York: Oxford University PressGoogle Scholar
  9. Binder-Macleod SA & Barker CB (1991). Use of a catch-like property of human skeletal muscle to reduce fatigue. Muscle & Nerve 14, 850–857.CrossRefGoogle Scholar
  10. Binder-Macleod SA & Guerin T (1990). Preservation of force output through progressive reduction of stimulation frequency in human quadriceps femoris muscle. Physical Therapy 70, 619–625.PubMedGoogle Scholar
  11. Botterman BR & Cope TC (1988). Motor-unit stimulation patterns during fatiguing contractions of constant tension. Journal of Neurophysiology 60, 1198–1214.PubMedGoogle Scholar
  12. Brownstone RM, Jordan LM, Kriellaars DJ, Noga BR & Shefchyk SJ (1992). On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Experimental Brain Research 90, 441–455.CrossRefGoogle Scholar
  13. Burke RE (1981). Motor units: anatomy, physiology, and functional organization. In: Brooks VB (ed.), Handbook of Physiology, Vol. II, Part 1, The Nervous System, pp 354–422. Bethesda: American Physiological Society.Google Scholar
  14. 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
  15. Capaday C, Cody FWJ & Stein RB (1990). Reciprocal inhibition of soleus motor output in humans during walking and voluntary tonic activity. Journal of Neurophysiology 64, 607–616.PubMedGoogle Scholar
  16. Clamann HP (1990). Changes that occur in motor units during activity. In: Binder MD, Mendell LM (eds.), The Segmental Motor System, pp. 239–257. New York: Oxford University Press.Google Scholar
  17. Dietz V (1992). Human neuronal control of automatic functional movements: interaction between central programs and afferent input. Physiological Reviews 72, 33–69.PubMedGoogle Scholar
  18. Dubose L, Schelhorn TB & Clamann HP (1987). Changes in contractile speed of cat motor units during activity. Muscle & Nerve 10, 744–752.CrossRefGoogle Scholar
  19. Dubuc R, Cabelguen J-M & Rossignol S (1988). Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat. Journal of Neurophysiology 60, 2014–2036.PubMedGoogle Scholar
  20. Dueñas SH, Loeb GE & Marks WB (1990). Monosynaptic and dorsal root reflexes during locomotion in normal and thalamic cats. Journal of Neurophysiology 63, 1467–1476.PubMedGoogle Scholar
  21. Edwards RHT, Wiles CM, Gohil K, Krywawych S & Jones DA (1982) Energy metabolism in human myopathy. In: Schotland DL (ed.), Disorders of the Motor Unit, pp. 715–726. New York: Wiley.Google Scholar
  22. Enoka RM & Stuart DG (1992). Neurobiology of muscle fatigue. Journal of Applied Physiology 72, 1631–1648.PubMedCrossRefGoogle Scholar
  23. Fitch S & McComas A (1985). Influence of human muscle length on fatigue. Journal of Physiology (London) 362, 205–213.Google Scholar
  24. Forssberg H, Grillner S & Rossignol S (1977). Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion. Brain Research 132, 121–139.PubMedCrossRefGoogle Scholar
  25. Fuglevand AJ, Zackowski KM, Huey KA & Enoka RM (1993). Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. Journal of Physiology (London) 260, 549–572.Google Scholar
  26. Gandevia SC (1993). Central and peripheral components to human isometric muscle fatigue. In: Sargeant AJ, Kernell D (eds.), Neuromuscular Fatigue, pp. 156-164. Amsterdam: Royal Netherlands Academy of Arts and Sciences.Google Scholar
  27. Gandevia SC, Macefield G, Burke D & McKenzie DK (1990). Voluntary activation of human motor axons in the absence of muscle afferent feedback. The control of the deafferented hand. Brain 113, 1563–1581.PubMedCrossRefGoogle Scholar
  28. Gandevia SC, Macefield VG, Bigland-Ritchie B, Gorman R & Burke D (1993). Motoneuronal output and gradation of effort in attempts to contract acutely paralyzed leg muscles in man. Journal of Physiology (London) 474, 411–427.Google Scholar
  29. Garland SJ, Gamer SH & McComas AJ (1988). Reduced voluntary electromyographic activity after fatiguing stimulation of human muscle. Journal of Physiology (London) 401, 547–556.Google Scholar
  30. Gelfand IM, Orlovsky GN & Shik ML (1988). Locomotion and scratching in tetrapods. In: Cohen AH, Rossignol S, Grillner S (eds.), Neural Control of Rhythmic Movements in Vertebrates, pp 167–199. New York: Wiley.Google Scholar
  31. Getting PA (1989). Emerging principles governing the operation of neural networks. Annual Review of Neuroscience 12, 185–204.PubMedCrossRefGoogle Scholar
  32. Gordon DA, Enoka RM & Stuart DG (1990). Motor-unit force potentiation in adult cats during a standard fatigue test. Journal of Physiology (London) 421, 569–582.Google Scholar
  33. Gossard J-P, Brownstone RM, Barajon I & Hultborn H (1994). Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat. Experimental Brain Research 98, 213–228.CrossRefGoogle Scholar
  34. Gossard J-P & Rossignol S (1990). Phase-dependent modulation of dorsal root potentials evoked by peripheral nerve stimulation during fictive locomotion in the cat. Brain Research 537, 1–13.PubMedCrossRefGoogle Scholar
  35. Graham-Brown T (1912). The factors in rhythmic activity of the nervous system. Proceedings Royal Society London B 85, 278–289.CrossRefGoogle Scholar
  36. Grillner S (1985). Neural control of vertebrate locomotion-central mechanisms and reflex interaction with special reference to the cat. In: Barnes WJP, Gladden MH (eds.), Feedback and Motor Control in Invertebrates and Vertebrates, pp. 35–56. London: Croom Helm.CrossRefGoogle Scholar
  37. Hamm TM, Sasaki SI, Stuart DG, Windhorst U & Yuan C-U (1987). Distribution of single-axon recurrent inhibitory post-synaptic potentials in a single spinal motor nucleus in the cat. Journal of Physiology (London) 388, 653–664.Google Scholar
  38. Harrison PJ & Jankowska E (1985). Sources of input to interneurones mediating group I non-reciprocal inhibition of motoneurones in the cat. Journal of Physiology (London) 361, 379–401.Google Scholar
  39. Hayward L, Breitbach D & Rymer WZ (1988). Increased inhibitory effects on close synergists during muscle fatigue in the decerebrate cat. Brain Research 440, 199–203.PubMedCrossRefGoogle Scholar
  40. Hayward L, Wesselmann U & Rymer WZ (1991). Effects of muscle fatigue on mechanically sensitive afferents of slow conduction velocity in the cat triceps surae. Journal of Neurophysiology 65, 360–370.PubMedGoogle Scholar
  41. Henneman E (1957). Relation between size of neurons and their susceptibility to discharge. Science 126, 1345–1346.PubMedCrossRefGoogle Scholar
  42. Houk JC & Rymer WZ (1981). Neural control of muscle length and tension. In: Brooks VB (ed.), Handbook of Physiology, Vol II, Part 1, The Nervous System, pp. 257–323. Bethesda: American Physiological Society.Google Scholar
  43. Houk JC, Singer JJ & Goldman MR (1970). An evaluation of length and force feedback to soleus muscles of decerebrate cats. Journal of Neurophysiology 33, 784–811.PubMedGoogle Scholar
  44. Jami L (1992). Golgi tendon organs in mammalian skeletal muscle: functional properties and central actions. Physiological Reviews 72, 623–666.PubMedGoogle Scholar
  45. Jankowska E (1992). Interneuronal relay in spinal pathways from proprioceptors. Progress in Neurobiology 38, 335–378.PubMedCrossRefGoogle Scholar
  46. Jankowska E, Johanisson T & Lipski J (1981). Common interneurons in reflex pathways from group Ia and Ib afferents of ankle extensors in the cat. Journal of Physiology (London) 310, 381–402.Google Scholar
  47. Jankowska E, Jukes MGM, Lund S & Lundberg A (1967a). The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiologica Scandinavica 70, 369–388.PubMedCrossRefGoogle Scholar
  48. Jankowska E, Jukes MGM, Lund S & Lundberg A (1967b). The effect of DOPA on the spinal cord. 6. Half-centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiologica Scandinavica 70, 389–402.PubMedCrossRefGoogle Scholar
  49. Kernell D (1992). Organized variability in the neuromuscular system: a survey of task-related adaptations. Archives Italiennes de Biologie 130, 19–66.PubMedGoogle Scholar
  50. Kernell D (1993) Neuromuscular fatigue and the differentiation of motoneurone and muscle unit properties. In: Sargeant AJ, Kernell D (eds.), Neuromuscular Fatigue, pp 139–146. Amsterdam: Royal Netherlands Academy of Arts and Sciences.Google Scholar
  51. Kernell D & Monster AW (1982). Motoneurone properties and motor fatigue. An intracellular study of gastrocnemius motoneurones of the cat. Experimental Brain Research 46, 197–204.Google Scholar
  52. Kirsch RF & Rymer WZ (1992). Neural compensation for fatigue-induced changes in muscle stiffness during perturbations of elbow angle in human. Journal of Neurophysiology 68, 449–470.PubMedGoogle Scholar
  53. Kukulka CG, Moore MA & Russell AG (1986). Changes in human a-motoneuron excitability during sustained maximum isometric contractions. Neuroscience Letters 68, 327–333.PubMedCrossRefGoogle Scholar
  54. Lenman AJR, Tulley FM, Vrbova G, Dimitrijevic MR & Towle JA (1989). Muscle fatigue in some neurological disorders. Muscle & Nerve 12, 938–942.CrossRefGoogle Scholar
  55. Macefield G, Hagbarth K-E, Gorman R, Gandevia SC & Burke D (1991). Decline in spindle support to a-motoneurones during sustained voluntary contractions. Journal of Physiology (London) 440, 497–512.Google Scholar
  56. Marsden CD, Meadows JC & Merton PA (1983). “Muscular wisdom” that minimizes fatigue during prolonged effort in man: peak rates of motoneuron discharge and slowing of discharge during fatigue. In: Desmedt JE (ed.), Motor Control Mechanisms in Health and Disease, pp. 169–211. New York: Raven Press.Google Scholar
  57. McKenzie DK, Bigland-Ritchie B, Gorman RB & Gandevia SC (1992). Central and peripheral fatigue of human diaphragm and limb muscles assessed by twitch interpolation. Journal of Physiology (London) 454, 643–656.Google Scholar
  58. Mense S (1986). Slowly conducting afferent fibers from deep tissues-neurobiological properties and central nervous actions. In: Ottoson D (ed.), Progress in Sensory Physiology, Vol. 6, pp. 139–219. Berlin: Springer-Verlag.Google Scholar
  59. Miller RG, Green AT, Moussavi RS, Carson PJ & Weiner MW (1990) Excessive muscular fatigue in patients with spastic paraparesis. Neurology 40, 1271–1274PubMedCrossRefGoogle Scholar
  60. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annual Review of Neuroscience 16, 265–297.PubMedCrossRefGoogle Scholar
  61. Pearson KG & Collins DF (1993). Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius muscle during locomotor activity. Journal of Neurophysiology 70, 1009–1017.PubMedGoogle Scholar
  62. Powers RK & Binder MD (1991). Effects of low-frequency stimulation on the tension-frequency relations of fast-twitch motor units in the cat. Journal of Neurophysiology 66, 905–918.PubMedGoogle Scholar
  63. Pratt CA & Jordan LM (1987). Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion. Journal of Neurophysiology 57, 56–71.PubMedGoogle Scholar
  64. Rotto DM & Kaufmann MP (1988). Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. Journal of Applied Physiology 64, 2306–2313.PubMedGoogle Scholar
  65. Rudomin P (1990). Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord. Trends in Neurosciences 13, 499–505.PubMedCrossRefGoogle Scholar
  66. Sillar KT (1991) Spinal pattern generation and sensory gating mechanisms. Current Opinion in Neurobiology 1, 583–589.PubMedCrossRefGoogle Scholar
  67. Sinoway LI, Hill, JM, Pickar, JG & Kaufman, MP (1993). Effects of contraction and lactic acid on the discharge of group III muscle afferents in cats. Journal of Neurophysiology 69, 1053–1059.PubMedGoogle Scholar
  68. Spielmann JM, Laouris Y, Nordstrom MA, Robinson GA, Reinking RM & Stuart DG (1993). Adaptation of cat motoneurons to sustained and intermittent extracellular activation. Journal of Physiology (Lon-don) 464, 75–120.Google Scholar
  69. Stuart DG & Callister RJ (1993). Afferent and spinal reflex aspects of muscle fatigue: issues and speculations. In: Sargeant AJ, Kernell D (eds), Neuromuscular Fatigue, pp. 169–180. Amsterdam: Royal Netherlands Academy of Arts and Sciences.Google Scholar
  70. Vøllestad NK, Sejersted OM, Bahr R, Woods JJ & Bigland-Ritchie B (1988). Motor drive and metabolic responses during repeated submaximal voluntary contractions in man. Journal of Applied Physiology 64, 1421–1427.PubMedGoogle Scholar
  71. Windhorst U (1988) How Brain-like is the Spinal Cord? Interacting Cell Assemblies in the Spinal Cord. Berlin: Springer-Verlag.CrossRefGoogle Scholar
  72. Windhorst U & Kokkoroyiannis T (1991). Interaction of recurrent inhibitory and muscle spindle afferent feedback during muscle fatigue. Neuroscience 43, 249–259.PubMedCrossRefGoogle Scholar
  73. Woods JJ, Furbush F & Bigland-Ritchie B (1987). Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. Journal of Neurophysiology 58, 125–137.PubMedGoogle Scholar
  74. Yang JF & Stein RB (1990). Phase-dependent reflex reversal in human leg muscles during walking. Journal of Neurophysiology 63, 1109–1117.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • U. Windhorst
    • 1
  • G. Boorman
    • 1
  1. 1.Departments of Clinical Neurosciences and Medical PhysiologyThe University of Calgary, Faculty of MedicineCalgaryCanada

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