Skip to main content

Role of Muscle Afferents in the Inhibition of Motoneurons During Fatigue

  • Chapter
Fatigue

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 384))

Abstract

In conscious humans, fatiguing muscular contractions are accompanied by a decrease in the discharge rate of alpha motoneurons. The association between alpha motoneuron discharge rate and the generation of force by skeletal muscle has been called “muscle wisdom” (Marsden et al., 1983). Its purpose is believed to ensure that central neural drive to skeletal muscle, which is fatigued, matches that needed to generate the required force. In addition, muscle wisdom may be one mechanism that functions either to decrease or to postpone central neural fatigue (Enoka & Stuart, 1992). Bigland-Ritchie and colleagues (1986) have suggested that a reflex arising from fatigued skeletal muscle is responsible, at least in part, for muscle wisdom. This chapter has two purposes. The first is to evaluate the evidence that a reflex arising from fatigued skeletal muscle causes muscle wisdom, and the second is to examine the discharge properties of muscle afferents to determine which ones are most likely to initiate reflexly this phenomenon.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andres KH, von During M & Schmidt RF (1985). Sensory innervation of the Achilles tendon by group III and IV afferent fibers. Anatomy and Embryology 172, 145–156.

    Article  PubMed  CAS  Google Scholar 

  • Balestra C, Cuchateau J & Hainaut K (1992). Effects of fatigue on the stretch reflex in a human muscle. Electroencephalography and Clinical Neurophysiology 85, 46–52.

    Article  PubMed  CAS  Google Scholar 

  • Bigland-Ritchie B (1981). EMG and fatigue of human voluntary and stimulated contractions. In: Porter R, Whelan J (eds.), Human Muscle Fatigue, Physiological Mechanisms, pp 130–156. London: Pitman Medical.

    Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Bigland-Ritchie B, Furbush F, Gandevia SC & Thomas CK (1992). Voluntary discharge frequencies of human motoneurons at different muscle lengths. Muscle & Nerve 15, 130–137.

    Article  CAS  Google Scholar 

  • Bongiovanni LG & Hagbarth K-E (1990). Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. Journal of Physiology (London) 423, 1–14.

    CAS  Google Scholar 

  • Boyd IA & Davy MR (1968). Composition of Peripheral Nerves. Edinbugh: Livingston.

    Google Scholar 

  • Burke D, Hagbarth K-E, Logstedt L & Wallin BG (1976). The response of human muscle spindle endings to vibration of non-contracting muscles. Journal of Physiology (London) 261, 695–711.

    CAS  Google Scholar 

  • Enoka RM & Stuart DG (1992). Neurobiology of muscle fatigue. Journal of Applied Physiology 72, 1631–1648.

    Article  PubMed  CAS  Google Scholar 

  • Gandevia SC, Macefield G, Burke D & McKenzie DK (1990). Voluntary activation of human motor axons in the absence of muscle afferent feedback. Brain 113, 1563–1581.

    Article  PubMed  Google Scholar 

  • Garland SJ. (1991). Role of small diameter afferents in reflex inhibition during human muscle fatigue. Journal of Physiology (London) 435, 547–558.

    CAS  Google Scholar 

  • Garland SJ, Garner SH & McComas AJ (1988). Reduced voluntary electromyographic activity after fatiguing stimulation of human muscle. Journal of Physiology (London) 408, 547–556.

    Google Scholar 

  • Garland SJ & McComas AJ (1990). Reflex inhibition of human soleus muscle during fatigue. Journal of Physiology (London) 429, 17–29.

    CAS  Google Scholar 

  • Hagbarth K-E, Kunesch EJ, Nordin M, Schmidt R & Wallin EU (1986). Gamma loop contributing to maximal voluntary contraction in man. Journal of Physiology (London) 380, 575–591.

    CAS  Google Scholar 

  • Hakkinen K & Komi PV (1983). Electromyographic and mechanical characteristics of human skeletal muscle during fatigue under voluntary and reflex conditions. Electroencephalography and Clinical Neuro-physiology (Limerick) 55, 436–444.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.(Abstract)

    PubMed  CAS  Google Scholar 

  • Hicks A & McComas AJ (1989). Increased sodium pump activity following repetitive stimulation of rat soleus muscles. Journal of Physiology (London) 414, 337–349.

    CAS  Google Scholar 

  • Hortobagyi T, Lambert NJ & Kroll WP (1991). Voluntary and reflex responses to fatigue with stretch-shortening exercise. Canadian Journal of Sport Sciences 16, 142–150.

    PubMed  CAS  Google Scholar 

  • Hunt CC (1954). Relation of function to diameter in afferent fibers of muscle nerves. Journal of General Physiology 38, 117–131.

    Article  PubMed  CAS  Google Scholar 

  • Hutton RS & Nelson DL (1986). Stretch sensitivity of Golgi tendon organs in fatigued gastrocnemius muscle. Medicine and Science in Sports and Exercise 1, 69–74.

    Google Scholar 

  • Jovanovic K, Anastasijevic R & Vuco J (1990). Reflex effects on gamma fusimotor neurones of chemically induced discharges in small diameter muscle afferents in decerebrate cats. Brain Research 521, 89–94.

    Article  PubMed  CAS  Google Scholar 

  • Kaufman MP, Longhurst JC, Rybicki KJ, Wallach JH & Mitchell JH (1983). Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. Journal of Applied Physiology 55, 105–112.

    PubMed  CAS  Google Scholar 

  • Kaufman MP, Rybicki KJ, Waldrop TG & Ordway GA (1984). Effect of ischemia on responses of group III and IV afferents to contraction. Journal of Applied Physiology 57, 644–650.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Kniffki K-D, Mense S & Schmidt RF (1978). Responses of group IV afferent units from skeletal muscle to stretch, contraction and chemical stimuli. Experimental Brain Research 31, 511–522.

    Article  CAS  Google Scholar 

  • Macefield VG, Gandevia SC, Bigland-Ritchie B, Gorman RB & Burke D (1993). The firing rates on human motoneurones voluntarily activated in the absence of muscle afferent feedback. Journal of Physiology (London) 471, 429–443.

    CAS  Google Scholar 

  • Macefield G, Hagbarth K-E, Gorman R, Gandevia SC & Burke D (1991). Decline in spindle support to alpha-motoneurones during sustained voluntary contractions. Journal of Physiology (London) 440, 497–512.

    CAS  Google Scholar 

  • 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 

  • Mense S (1977). Nervous outflow from skeletal muscle following chemical noxious stimulation. Journal of Physiology (London) 267, 75–88.

    CAS  Google Scholar 

  • Mense S (1981). Sensitization of group IV muscle receptors to bradykinin by 5-hydroxytryptamine and prostaglandin E-2. Brain Research 225, 95–105.

    Article  PubMed  CAS  Google Scholar 

  • Mense S & Meyer H (1988). Bradykinin-induced modulation of the response behavour of different types of feline group III and IV muscle receptors. Journal of Physiology (London) 398, 49–63.

    CAS  Google Scholar 

  • Mense S & Schmidt RF (1974). Activation of group IV afferent units from muscle by algesic agents. Brain Research 72, 305–310.

    Article  PubMed  CAS  Google Scholar 

  • Mense S & Stahnke M (1983). Responses in muscle afferent fibers of slow conduction velocity to contractions and ischemia in the cat. Journal of Physiology (London) 342, 383–397.

    CAS  Google Scholar 

  • Nelson DL & Hutton RS (1985). Dynamic and static stretch responses in muscle spindle receptors in fatigued muscle. Medicine and Science in Sports and Exercise 17, 45–450 (Abstract)

    Google Scholar 

  • Prochazka A & Somjen GG (1986). Insensitivity of cat muscle spindles to hyperkalaemia in the physiological range. Journal of Physiology (London) 372, 26P.

    Google Scholar 

  • Rotto DM & Kaufman MP (1988). Effects of metabolic products of muscular contraction on the discharge of group III and IV afferents. Journal of Applied Physiology 64, 2306–2313.

    PubMed  CAS  Google Scholar 

  • Rotto DM, Massey KD, Burton KP & Kaufman MP (1989). Static contraction increases arachidonic acid levels in gastrocnemius muscles of cats. Journal of Applied Physiology 66, 2721–2724.

    PubMed  CAS  Google Scholar 

  • Rotto DM, Schultz HD, Longhurst JC & Kaufman MP (1990). Sensitization of group III muscle afferents to static contraction by products of arachidonic acid metabolism. Journal of Applied Physiology 68, 861–867.

    PubMed  CAS  Google Scholar 

  • Rybicki KJ, Waldrop TG & Kaufman MP (1985). Increasing gracilis interstitial potassium concentrations stimulates group III and IV afferents. Journal of Applied Physiology 58, 936–941.

    Article  PubMed  CAS  Google Scholar 

  • Sharpe MH & Miles TS (1993). Position sense at the elbow after fatiguing contractions. Experimental Brain Research 94, 179–182.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Stebbins CL, Carretero OA, Mindroiu T & Longhurst JC (1990). Bradykinin release from contracting skeletal muscle of the cat. Journal of Applied Physiology 69, 1225–1230.

    PubMed  CAS  Google Scholar 

  • Thimm F & Baum K (1987). Response of chemosensitive nerve fibers of group III and IV to metabolic changes in rat muscles. Pflügers Archiv 410, 143–152.

    Article  PubMed  CAS  Google Scholar 

  • von During M & Andres KH (1990). Topography and ultrastructure of group III and IV nerve terminals of cat’s gastrocnemius-soleus muscle. In: Zenker W, Neuhuber WL (eds.), The Primary Afferent Neuron: A Survey of Recent Morpho-Functional Aspects, New York: Plenum.

    Google Scholar 

  • Windhorst U & Kokkoroyiannis T (1991). Interaction of recurrent inhibitory and muscle spindle afferent feedback during muscle fatigue. Neuroscience 43, 249–259.

    Article  PubMed  CAS  Google Scholar 

  • Woods J, Furbush F & Bigland-Ritchie B (1987). Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. Journal of Neurophysiology 58, 125–137.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer Science+Business Media New York

About this chapter

Cite this chapter

Garland, S.J., Kaufman, M.P. (1995). Role of Muscle Afferents in the Inhibition of Motoneurons During Fatigue. In: Gandevia, S.C., Enoka, R.M., McComas, A.J., Stuart, D.G., Thomas, C.K., Pierce, P.A. (eds) Fatigue. Advances in Experimental Medicine and Biology, vol 384. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-1016-5_21

Download citation

  • DOI: https://doi.org/10.1007/978-1-4899-1016-5_21

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4899-1018-9

  • Online ISBN: 978-1-4899-1016-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics