Abstract
Several lines of evidence point to an important role of the rusimotor system in the “muscle-wisdom” phenomenon during peripheral fatigue of some human voluntary contractions: 1) muscle afferents provide a net amplification of skeletomotor output, with the only known afferent species capable of this being the muscle spindle; 2) muscle spindle firing rates decline during constant-force voluntary contractions, so fusimotor support to skeletomotor output decreases; 3) this waning support can be offset by application of high-frequency vibration to the fatiguing muscle, which excites spindle endings; and 4) the progressive decline in motor unit firing rates during maximal voluntary contractions is abolished by blocking muscle afferent inputs, and it is argued that, at least in the initial stages of a contraction, this must be due to a progressive withdrawal of spindle support.
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References
Anastasijevic R, Jovanovic K & Ljubisavljevic M (1995). Fusimotor responses to fatiguing contractions of a muscle in non-denervated cat hindlimb. In: Stuart DG, Gantchev GN, Gurfinkel VS, Wiesendanger M (eds.), Motor Control VII, pp. 00-00. Tucson: Motor Control Press. In press
Aniss AM, Diener HC, Hore J, Burke D & Gandevia SC (1990). Reflex activation of muscle spindles in human pretibial muscles during standing. Journal of Neurophysiology 64, 671–679.
Appelberg B, Hulliger M, Johansson H & Sojka P (1983). Actions on gamma-motoneurones elicited by electrical stimulation of group III muscle afferents in the hind limb of the cat. Journal of Physiology (London) 335, 275–292.
Baldissera F & Pierrot-Deseilligny E (1989). Facilitation of transmission in the pathway of non-monosynaptic Ia excitation to wrist flexor motoneurones at the onset of voluntary movement in man. Experimental Brain Research 74, 437–439.
Balestra C, Duchateau J & Hainaut K (1992). Effects of fatigue on the stretch reflex in a human muscle. Electroencephalography and Clinical Neurophysiology 85, 46–52.
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.
Bigland-Ritchie B, Cafarelli E & Vøllestad NK (1986). Fatigue of submaximal static contractions. Acta Physiologica Scandinavia Supplement 556, 137–148.
Bigland-Ritchie B, Johansson R, Lippold OCJ, Smith S & Woods JJ (1983). Changes in motoneurone firing rates during sustained maximal voluntary contractions. Journal of Physiology (London) 340, 335–346.
Bigland-Ritchie B, Jones DA & Woods JJ (1979). Excitation frequency and muscle fatigue: electrical responses during voluntary and stimulated contractions. Experimental Neurology 64, 414–427.
Bigland-Ritchie B & Woods JJ (1984). Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle & Nerve 7, 691–699.
Bigland-Ritchie BR, Dawson NJ, Johansson RS & Lippold OC (1986). Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. Journal of Physiology (London) 379, 451–459.
Bigland-Ritchie BR, Furbush FH, Gandevia SC & Thomas CK (1992). Voluntary discharge frequencies of human motoneurons at different muscle lengths. Muscle & Nerve 15, 130–137.
Binder-Macleod SA & Guerin T (1990). Preservation of force output through progressive reduction of stimulation frequency in human quadriceps femoris muscle. Physical Therapeutics 70, 619–625.
Bongiovanni LG & Hagbarth KE (1990). Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. Journal of Physiology (London) 423, 1–14.
Bongiovanni LG, Hagbarth KE & Stjernberg L (1990). Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man. Journal of Physiology (London) 423, 15–26.
Burke D (1981). The activity of human muscle spindle endings during normal motor behavior. In: Porter R (ed.), Neurophysiology IV. International Review of Physiology, pp. 91–126. Baltimore, MD: University Park Press.
Burke D, Gracies JM, Meunier S & Pierrot-Deseilligny E (1992). Changes in presynaptic inhibition of afferents to propriospinal-like neurones in man during voluntary contractions. Journal of Physiology (London) 449, 673–687.
Cleland C, Rymer W & Edwards F (1982). Force-sensitive interneurones in the spinal cord of the cat. Science 217, 652–655.
Darling WG & Hayes KC (1983). Human servo responses to load disturbances in fatigued muscle. Brain Research 267, 345–351.
Duchateau J & Hainaut K (1993). Behaviour of short and long latency reflexes in fatigued human muscles. Journal of Physiology (London) 471, 787–799.
Eldred E, Granit R & Merton PA (1953). Supraspinal control of the muscle spindles and its significance. Journal of Physiology (London) 122, 498–523.
Enoka RM & Stuart DG (1992). Neurobiology of muscle fatigue. Journal of Applied Physiology 72, 1631–1648.
Gandevia SC, Burke D, Macefield G & McKenzie DK (1992). Human motor output, muscle fatigue and muscle afferent feedback. Proceedings of the Australian Physiological and Pharmacological Society 23, 59–67.
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.
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.
Garland SJ (1991). Role of small diameter afferents in reflex inhibition during human muscle fatigue. Journal of Physiology (London) 435, 547–558.
Garland SJ, Garner SH & McComas AJ (1988). Reduced voluntary electromyographic activity after fatiguing stimulation of human muscle. Journal of Physiology (London) 401, 547–556.
Garland SJ & McComas AJ (1990). Reflex inhibition of human soleus muscle during fatigue. Journal of Physiology (London) 429, 17–27.
Gregory JE, Mark RF, Morgan DL, Patak A, Polus B & Proske U (1990). Effects of muscle history on the stretch reflex in cat and man. Journal of Physiology (London) 424, 93–107.
Gregory JE, Morgan DL & Proske U (1987). Changes in size of the stretch reflex of cat and man attributed to aftereffects in muscle spindles. Journal of Neurophysiology 58, 628–640.
Grimby L, Hannerz J & Hedman B (1981). The fatigue and voluntary discharge properties of single motor units in man. Journal of Physiology (London) 316, 545–554.
Hagbarth KE (1993). Microneurography and applications to issues of motor control: Fifth Annual Stuart Reiner Memorial Lecture. Muscle & Nerve 16, 693–705.
Hagbarth KE, Kunesch EJ, Nordin M, Schmidt R & Wallin EU (1986). Gamma loop contributing to maximal voluntary contractions in man. Journal of Physiology (London) 380, 575–591.
Hagbarth KE, Nordin M & Bongiovanni LG (1995). After-effects on stiffness and stretch reflexes of human finger flexor muscles attributed to muscle thixotropy. Journal of Physiology (London) 482.1, 215–223.
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.
Hultborn H, Meunier S, Pierrot-Deseilligny E & Shindo M (1987). Changes in presynaptic inhibition of Ia fibres at the onset of voluntary contraction in man. Journal of Physiology (London) 389, 757–772.
Hunter IW & Kearney RE (1983). Invariance of ankle dynamic sensitivity during fatiguing muscle contractions. Journal of Biomechanics 16, 985–991.
Häkkinen K & Komi PV (1983). Electromyographic and mechanical characteristics of human skeletal muscle during fatigue under voluntary and reflex conditions. Electroencephalography and Clinical Neurophysiology 55, 436–444.
Johansson H, Djupsjöbacka M & Sjölander P (1993). Influences on the gamma-muscle spindle system from muscle afferents stimulated by KC1 and lactic acid. Neuroscience Research 16, 49–57.
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.
Kaufman MP, Longhurst JC, Rybicki KJ, Wallach JH & Mitchell JH (1983). Effects of static muscular contraction on impulse activity in groups III and IV afferents in cats. Journal of Applied Physiology 55, 105–112.
Kirsch RF & Rymer WZ (1987). Neural compensation for muscular fatigue: evidence for significant force regulation in man. Journal of Neurophysiology 57, 1893–1910.
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.
Kniffki KD, Mense S & Schmidt RF (1978). Responses of group IV afferent units from muscle to stretch, contraction and chemical stimulation. Experimental Brain Research 31, 511–522.
Kniffki KD, Shomburg ED & Steffens, H (1981). Synaptic effects from chemically activated fine muscle afferents upon alpha motoneurones in decerebrate and spinal cats. Brain Research 206, 361–370.
Kukulka CG, Moore MA & Russell AG (1986). Changes in human alpha-motoneuron excitability during sustained maximum isometric contractions. Neuroscience Letters 68, 327–333.
Kumazawa T & Mizumura K (1977). Thin-fibre receptors responding to mechanical, chemical and thermal stimuli in the skeletal muscle of the dog. Journal of Physiology (London) 273, 179–194.
Lagier-Tessonnier F, Balzamo E & Jammes Y (1993). Comparative effects of ischemia and acute hypoxemia on muscle afferents from tibialis anterior in cats. Muscle & Nerve 16, 135–141.
Ljubisavljevic M, Jovanovic K & Anastasijevic R (1992a). Changes in discharge rate of cat hamstring fusimotor neurones during fatiguing contractions of triceps surae muscles. Brain Research 579, 246–252.
Ljubisavljevic M, Jovanovic K & Anastasijevic R (1992b). Changes in discharge rate of fusimotor neurones provoked by fatiguing contractions of cat triceps surae muscles. Journal of Physiology (London) 445, 499–513.
Ljubisavljevic M & Anastasijevic R (1995). Muscle spindle afferent discharges during fatiguing muscle contractions in decerebrate cats. In: Stuart DG, Gantchev GN, Gurfinkel VS, Wiesendanger M (eds.), Motor Control VII, pp. 00-00. Tucson AZ: Motor Control Press. In press
Loeb GE & Hoffer JA (1981). Muscle spindle function during normal and disturbed locomotion. In: Taylor A, Prochazka A (eds.), Muscle Receptors and Movement, pp. 219–228. London: Macmillan.
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.
Macefield VG, Gandevia SC, Bigland-Ritchie B, Gorman R & Burke D (1993). The firing rates of human motoneurones voluntarily activated in the absence of muscle afferent feedback. Journal of Physiology (London) 474, 429–443.
Marsden CD, Meadows JC & Merton PA (1983) “Muscular wisdom” that minimized 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.
Matthews PB (1986). Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. Journal of Physiology (London) 374, 73–90.
Matthews PBC (1981). Evolving views on the internal operation and functional role of the muscle spindle. Journal of Physiology (London) 320, 1–30.
Mense S & Stahnke M (1983). Responses in muscle afferent fibres of slow conduction velocity to contractions and ischaemia in the cat. Journal of Physiology (London) 342, 383–397.
Merton PA (1953). Speculations on the servo-control of movement. In: Wolstenholme, GEW (ed.), The Spinal Cord, pp. 247–307. London: Churchill.
Merton PA (1954). Voluntary strength and fatigue. Journal of Physiology (London) 123, 553–564.
Meunier S & Pierrot-Deseilligny E (1989). Gating of the afferent volley of the monosynaptic stretch reflex during movement in man. Journal of Physiology (London) 419, 753–763.
Nelson DL & Hutton RS (1985). Dynamic and static stretch responses in muscle spindle receptors in fatigued muscle. Medicine and Science in Sports Exercise 17, 445–450.
Person RS (1974). Rhythmic activity in a group of human motoneurones during voluntary contraction of a muscle. Electroencephalography and Clinical Neurophysiology 36, 585–595.
Polus BI, Patak A, Gregory JE & Proske U (1991). Effect of muscle length on phasic stretch reflexes in humans and cats. Journal of Neurophysiology 66, 613–622.
Prochazka A & Wand P (1981). Independence of fusimotor and skeletomotor systems during voluntary movements. In: Taylor A, Prochazka A (eds.), Muscle Receptors and Movement, pp. 229–243. London: Macmillan.
Ribot-Ciscar E, Tardy-Gervet MF, Vedel JP & Roll JP (1991). Post-contraction changes in human muscle spindle resting discharge and stretch sensitivity. Experimental Brain Research 86, 673–678.
Rotto DM & Kaufman MP (1988). Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. Journal of Applied Physiology 64, 2306–2313.
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.
Vallbo ÅB, Hagbarth K-E, Torebjörk HE & Wallin BG (1979). Somatosensory, proprioceptive and sympathetic activity in human peripheral nerves. Physiological Reviews 59, 919–957.
Windhorst U, Christakos CN, Koehler W, Hamm TM, Enoka RM & Stuart DG (1986). Amplitude reduction of motor unit twitches during repetitive activation is accompanied by relative increase of hyperpolarizing membrane potential trajectories in homonymous alpha-motoneurons. Brain Research 398, 181–184.
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.
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Hagbarth, KE., Macefield, V.G. (1995). The Fusimotor System. 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_20
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DOI: https://doi.org/10.1007/978-1-4899-1016-5_20
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