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Exercise, fatigue and proprioception: a retrospective

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This is an account of experiments carried out in my laboratory over more than 20 years, exploring the influence of exercise on human limb position sense. It is known that after intense exercise we are clumsy in the execution of skilled movements. The first question we posed concerned eccentric exercise, where the contracting muscle is forcibly lengthened. Such exercise produces muscle damage, and the damage might extend to the muscle’s proprioceptors, the muscle spindles, producing a disturbance of limb position sense. However, provided the exercise was sufficiently severe (20–30% fall in muscle force), comparing eccentric exercise with concentric exercise, where no damage ensues, there was no difference in the effects on position sense. After exercise of elbow muscles, the forearm was always perceived as more extended than its actual position. It led to a new hypothesis: after exercise, did the extra effort required to lift the fatigued arm provide a position signal? Findings based on spindles’ thixotropic behaviour did not support such a proposition for the elbow joint, although at the wrist an effort signal may contribute. Spindle thixotropy has also been proposed to explain the poor proprioception experienced under conditions of weightlessness. After exercise of elbow extensors or flexors, the position errors were always in the direction of forearm extension. At the knee, after exercise the lower leg was always perceived as more flexed. These findings led to the conclusion that disturbances to position sense, post-exercise, did not involve peripheral receptors, and that the effect arose within the brain.

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Fig. 1

Redrawn from Tsay et al. (2016)

Fig. 2

Redrawn from Allen et al. (2007)

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References

  • Adamovich SV, Berkinblit MB, Fookson O, Poizner H (1998) Pointing in 3D space to remembered targets. 1. Kinesthetic versus visual target presentation. J Neurophysiol 79:2833–2846

    Article  CAS  PubMed  Google Scholar 

  • Allen TJ, Proske U (2006) Effect of muscle fatigue on the sense of limb position and movement. Exp Brain Res 170:30–38

    Article  CAS  PubMed  Google Scholar 

  • Allen TJ, Ansems GE, Proske U (2007) Effects of muscle conditioning on position sense at the human forearm during loading or fatigue of elbow flexors and the role of the sense of effort. J Physiol 580:423–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen TJ, Leung M, Proske U (2010) The effect of fatigue from exercise on human limb position sense. J Physiol 588(8):1369–1377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen TJ, Jones T, Tsay A, Morgan DL, Proske U (2018) Muscle damage produced by isometric contractions in human elbow flexors. J Appl Physiol 124:388–399

    Article  PubMed  Google Scholar 

  • Ansems GE, Allen TJ, Proske U (2006) Position sense at the human forearm in the horizontal plane during loading and vibration of elbow muscles. J Physiol 576:445–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bastian HC (1880) The brain as an organ of the mind. Appleton, New York

    Google Scholar 

  • Bhanpuri NH, Okamura AM, Bastian AJ (2012) Active force perception depends on cerebellar function. J Neuophysiol 107:1612–1620

    Article  Google Scholar 

  • Bhanpuri NH, Okamura AM, Bastian AJ (2013) Predictive modelling by the cerebellum improves proprioception. J Neurosci 33(36):14301–14306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bringoux L, Blouin J, Coyle T, Ruget H, Mouchnino L (2012) Effect of gravity-like torque on goal-directed arm movements in microgravity. J Neurophysiol 107:2541–2548

    Article  CAS  PubMed  Google Scholar 

  • Brockett C, Warren N, Gregory JE, Morgan DL, Proske U (1997) A comparison of the effects of concentric versus eccentric exercise on force and position sense at the human elbow joint. Brain Res 771:251–258

    Article  CAS  PubMed  Google Scholar 

  • Capaday C, Cooke JD (1981) The effects of muscle vibration on the attainment of intended final position during voluntary human arm movements. Exp Brain Res 42:228–230

    Article  CAS  PubMed  Google Scholar 

  • Capaday C, Cooke JD (1983) Vibration induced changes in movement-related EMG activity in humans. Exp Brain Res 52:139–146

    Article  CAS  PubMed  Google Scholar 

  • Capaday C, Darling WG, Stanek K, Van Vreeswijk C (2013) Pointing to oneself: active versus passive proprioception revisited and implications for internal models of motor system function. Exp Brain Res 229:171–180

    Article  PubMed  Google Scholar 

  • Clark FJ, Burgess RC, Chapin JW (1986) Proprioception with the proximal interphalangeal joint of the index finger. Evidence for a movement sense without a static-position sense. Brain 109(6):1195–1208

    Article  PubMed  Google Scholar 

  • Cole J (1995) Pride and a daily marathon. MIT Press, Boston

    Google Scholar 

  • Cole J (2007) The phenomenology of agency and intention in the face of paralysis and insentience. Phenom Cogn Sci 6:309–325

    Article  Google Scholar 

  • Collins DF, Refshauge KM, Todd G, Gandevia SC (2005) Cutaneous receptors contribute to kinaesthesia at the index finger, elbow and knee. J Neurophysiol 94:1699–1706

    Article  CAS  PubMed  Google Scholar 

  • Cordo P, Carlton L, Bevan L, Carlton M, Kerr GK (1994) Proprioceptive coordination of movement sequences: role of velocity and position information. J Neurophysiol 71(5):1848–1861

    Article  CAS  PubMed  Google Scholar 

  • Cullen KE (2004) Sensory signals during active versus passive movement. Curr Opin Neurobiol 14:698–706

    Article  CAS  PubMed  Google Scholar 

  • Darling WG, Wall BM, Coffman CR, Capaday C (2018) Pointing to one’s moving hand: putative internal models do not contribute to proprioceptive acuity. Front Hum Neurosci 12(177):1–13

    Google Scholar 

  • Day BL, Fitzpatrick RC (2005) Virtual head rotation reveals a process of route reconstruction from human vestibular signals. J Physiol 567(2):591–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrell WR, Smith A (1988) Position sense at the proximal interphalangeal joint of the human index finger. J Physiol 399:49–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forestier N, Teasdale N, Nougier V (2002) Alteration of the position sense at the ankle induced by muscular fatigue in humans. Med Sci Sports Exerc 34(1):117–122

    Article  PubMed  Google Scholar 

  • Fuentes CT, Bastian A (2010) Where is your arm? Variations of proprioception across space and tasks. J Neurophysiol 103:164–171

    Article  PubMed  Google Scholar 

  • Gandevia SC, Smith JL, Crawford M, Proske U, Taylor JL (2006) Motor commands contribute to human position sense. J Physiol 571:703–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilhodes JC, Roll JP, Tardy-Gervet MF (1986) Perceptual and motor effects of agonist-antagonist muscle vibration in man. Exp Brain Res 61:395–402

    Article  CAS  PubMed  Google Scholar 

  • Givoni NJ, Pham T, Allen TJ, Proske U (2007) The effect of quadriceps muscle fatigue on position matching at the knee. J Physiol 584:111–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gladden MH (1976) Structural features relative to the function of intrafusal muscle fibres in the cat. Prog Brain Res 44:51–59

    Article  CAS  PubMed  Google Scholar 

  • Goodwin GM, McCloskey DI, Matthews PB (1972) The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 95:705–748

    Article  CAS  PubMed  Google Scholar 

  • Gooey K, Bradfield O, Talbot J, Morgan DL, Proske U (2000) Effects of body orientation, load and vibration on sensing position and movement at the human elbow joint. Exp Brain Res 133:340–348

    Article  CAS  PubMed  Google Scholar 

  • Gregory JE, Morgan DL, Proske U (1988) After-effects in the responses of cat muscle spindles and errors in limb position sense in man. J Neurophysiol 59:1220–1230

    Article  CAS  PubMed  Google Scholar 

  • Gregory JE, Brockett CL, Morgan DL, Whitehead NP, Proske U (2002) Effects of eccentric muscle contractions on Golgi tendon organ responses to passive and active tension in the cat. J Physiol 538(1):209–218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory JE, Morgan DL, Proske U (2004) Responses of muscle spindles following a series of eccentric contractions. Exp Brain Res 157:234–240

    Article  CAS  PubMed  Google Scholar 

  • Hall LA, McCloskey DI (1983) Detection of movements imposed on finger, elbow and shoulder joints. J Physiol 335:519–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill DK (1968) Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation. J Physiol 199:637–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inglis JT, Frank JS (1990) The effect of agonist/antagonist muscle vibration on human position sense. Exp Brain Res 81:573–580

    Article  CAS  PubMed  Google Scholar 

  • Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727

    Article  CAS  PubMed  Google Scholar 

  • Lackner JR, DiZio P (1992) Gravitoinertial force level affects the appreciation of limb position during muscle vibration. Brain Res 592:175–180

    Article  CAS  PubMed  Google Scholar 

  • Lakie M, Walsh EG, Wright GW (1984) Resonance at the wrist demonstrated by the use of a torque motor: an instrumental analysis of muscle tone in man. J Physiol 353:265–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lattanzio P-J, Petrella RJ, Sproule JR, Fowler PJ (1997) Effects of fatigue on knee proprioception. Clin J Sport Med 7:22–27

    Article  CAS  PubMed  Google Scholar 

  • Longo MR, Haggard P (2010) An implicit body representation underlying human position sense. Proc Natl Acad Sci USA 107:11727–11732

    Article  PubMed  Google Scholar 

  • Matthews PBC (1972) Mammalian muscle receptors and their central actions. Edward Arnold, London

    Google Scholar 

  • Matthews PBC (1982) Where does Sherrington’s “Muscular sense” originate? Muscles, joints, corollary discharges? Ann Rev Neurosci 5:189–218

    Article  CAS  PubMed  Google Scholar 

  • McCloskey DI (1973) Differences between the senses of position and movement shown by the effects of loading and vibration of muscles in man. Brain Res 61:119–131

    Article  CAS  PubMed  Google Scholar 

  • McCloskey DI (1981) Corollary discharges: motor commands and percepsion. In: Brookhart JM, Mountcastle VB (eds) Handbook of physiology, The nervous system. Motor control, sect 1, vol II, Pt 2, chap 32, American Physiological Society, Bethesda, pp 1415–1447

  • McCloskey DI, Cross MJ, Honner R, Potter EK (1983) Sensory effects of pulling or vibrating exposed tendons in man. Brain 106(Pt 1):21–37

    Article  PubMed  Google Scholar 

  • Morgan DL, Prochazka A, Proske U (1984) The after-effects of stretch and fusimotor stimulation on the responses of primary endings of cat muscle spindles. J Physiol 356:465–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paillard J, Brouchon M (1968) Active and passive movements in the calibration of position sense. In: Freedman SJ (ed) The neuropsychology of spatially oriented behaviour, vol III, chap 3. Dorsey Press, Homewood 37–55

    Google Scholar 

  • Pedersen JM, Ljubislavlevic M, Bergenheim M, Johansson H (1998) Alterations in information transmission in ensemble of primary muscle spindle afferents after muscle fatigue in heteronymous muscle. Neuroscience 84:953–959

    Article  CAS  PubMed  Google Scholar 

  • Pedersen JM, Lonn J, Hellstrom F, Djupsjobacka M, Johansson H (1999) Localised muscle fatigue decreases the acuity of the movement sense in the human shoulder. Med Sci Sports Exerc 31(7):1047–1052

    Article  CAS  PubMed  Google Scholar 

  • Proske U, Allen TJ (2019) The neural basis of the senses of effort, force and heaviness. Exp Brain Res 237:589–599

    Article  PubMed  Google Scholar 

  • Proske U, Gandevia SC (2012) The proprioceptive senses: their roles in signalling body shape, body position and movement, and muscular force. Physiol Rev 92(4):1651–1697

    Article  CAS  PubMed  Google Scholar 

  • Proske U, Gandevia SC (2018) Kinesthetic senses. Compr Physiol 8:1157–1183

    Article  PubMed  Google Scholar 

  • Proske U, Morgan DL (2001) Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 537:333–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Proske U, Morgan DL, Gregory JE (1993) Thixotropy in skeletal muscle and in muscle spindles: a review. Prog Neurobiol 41(6):705–721

    Article  CAS  PubMed  Google Scholar 

  • Proske U, Tsay A, Allen TJ (2014) Muscle thixotropy as a tool in the study of proprioception. Exp Brain Res 232:3397–3412

    Article  PubMed  Google Scholar 

  • Ribeiro F, Mota J, Oliveira J (2007) Effect of exercise-induced fatigue on position sense of the knee in the elderly. Eur J Physiol 99:379–385

    Article  Google Scholar 

  • Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76:213–222

    Article  CAS  PubMed  Google Scholar 

  • Roll R, Gilhodes JC, Roll JP, Popov K, Charade O, Gurfinkel V (1998) Proprioceptive information processing in weightlessness. Exp Brain Res 122:393–402

    Article  CAS  PubMed  Google Scholar 

  • Saradjian AH, Tremblay L, Perrier J, Blouin J, Mouchnino L (2013) Cortical facilitation of proprioceptive inputs related to gravitational balance constraints during step preparation. J Neurophysiol 110:397–407

    Article  PubMed  Google Scholar 

  • Saxton JM, Clarkson PM, James R, Miles M, Westerfer M, Clark S, Donnelly AE (1995) Neuromuscular dysfunction following eccentric exercise. Med Sci Sports Exerc 27:1185–1193

    Article  CAS  PubMed  Google Scholar 

  • Sharpe MH, Miles TS (1993) Position sense at the elbow after fatiguing contractions. Exp Brain Res 94:179–182

    Article  CAS  PubMed  Google Scholar 

  • Sittig AC, Denier van der Gon JJ, Gielen CC (1985) Separate control of arm position and velocity demonstrated by vibration of muscle tendon in man. Exp Brain Res 60:445–453

    Article  CAS  PubMed  Google Scholar 

  • Skinner HB, Wyatt MP, Hodgdon JA, Conard DW, Barrack RL (1986) Effect of fatigue on joint position sense of the knee. J Orthop Res 4:112–118

    Article  CAS  PubMed  Google Scholar 

  • Smith ICH, Newham DJ (2007) Fatigue and functional performance of human biceps muscle following concentric or eccentric contractions. J Appl Physiol 102:207–213

    Article  PubMed  Google Scholar 

  • Smith JL, Cawford M, Proske U, Taylor JL, Gandevia SC (2009) Signals of motor command bias joint position sense in the presence of feedback from proprioceptors. J Appl Physiol 106:950–958

    Article  PubMed  Google Scholar 

  • Taylor JL, McCloskey DI (1992) Detection of slow movements imposed at the elbow during active flexion in man. J Physiol 457:503–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsay A, Allen TJ, Leung M, Proske U (2012) The fall in force after exercise disturbs position sense at the human forearm. Exp Brain Res 222:415–425

    Article  PubMed  Google Scholar 

  • Tsay A, Savage G, Allen TJ, Proske U (2014) Limb position sense, proprioceptive drift and muscle thixotropy at the human elbow joint. J Physiol 592:2679–2694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsay A, Giummarra MJ, Allen TJ, Proske U (2016) The sensory origins of human position sense. J Physiol 594:1037–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vallbo AB (1971) Muscle spindle responses at the onset of isometric voluntary contractions in man. Time difference between fusimotor and skeletomotor effects. J Physiol 218:405–431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vallbo AB (1974) Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque. Acta Physiol Scand 90:319–336

    Article  CAS  PubMed  Google Scholar 

  • Von Holst H, Mittelstaedt H (1950) The reafference principle. In: Selected papers of Erich von Holst. “The behavioural physiology of animals and man”. (trans: German by Martin R, 1973), Methuen, London pp 139–173

  • Walsh LD, Hesse CW, Morgan DL, Proske U (2004) Human forearm position sense after fatigue of elbow flexor muscles. J Physiol 558:705–715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh LD, Allen TJ, Gandevia SC, Proske U (2006) Effect of eccentric exercise on position sense at the human forearm in different postures. J Appl Physiol 100:1109–1116

    Article  CAS  PubMed  Google Scholar 

  • Walsh LD, Smith JL, Gandevia SC, Taylor JL (2009) The combined effect of muscle contraction history and motor commands on human position sense. Exp Brain Res 195:603–610

    Article  PubMed  Google Scholar 

  • Walsh LD, Proske U, Allen TJ, Gandevia SC (2013) The contribution of motor commands to position sense differs between elbow and wrist. J Physiol 591:6103–6114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winter JA, Allen TJ, Proske U (2005) Muscle spindle signals combine with the sense of effort to indicate limb position. J Physiol 568:1035–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wise AK, Gregory JE, Proske U (1998) Detection of movements of the human forearm during and after co-contractions of muscles acting at the elbow joint. J Physiol 508(1):325–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wise AK, Gregory JE, Proske U (1999) The responses of muscle spindles to small, slow movements in passive muscle and during fusimotor activity. Brain Res 821:87–94

    Article  CAS  PubMed  Google Scholar 

  • Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880–1882

    Article  CAS  PubMed  Google Scholar 

  • Worringham CJ, Stelmach GE (1985) The contribution of gravitational torques to limb position sense. Exp Brain Res 61:38–42

    Article  CAS  PubMed  Google Scholar 

  • Young LR, Oman CM, Merfeld D, Watt D, Roy S, De Luca C, Blackwill D, Christie J, Grolean N, Jackson DK, Low G, Modestino S, Mayer W (1993) Spatial orientation and posture during and following weightlessness: human experiments on Spacelab life sciences. J Vestib Res 3:231–239

    CAS  PubMed  Google Scholar 

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Acknowledgements

I would like to thank Trevor Allen for his help with preparation of the manuscript and illustrations, Florian Monjo for his comments on parts of the text, and all of my collaborators over the years who contributed to the work, most of whose names appear as co-authors in the published papers.

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  1. Department of Physiology, Monash University, Clayton, VIC, 3800, Australia

    Uwe Proske

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Proske, U. Exercise, fatigue and proprioception: a retrospective. Exp Brain Res 237, 2447–2459 (2019). https://doi.org/10.1007/s00221-019-05634-8

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