Experimental Brain Research

, Volume 183, Issue 2, pp 235–240 | Cite as

Tongue-placed tactile biofeedback suppresses the deleterious effects of muscle fatigue on joint position sense at the ankle

  • Nicolas Vuillerme
  • Matthieu Boisgontier
  • Olivier Chenu
  • Jacques Demongeot
  • Yohan Payan
Research Article


Whereas the acuity of the position sense at the ankle can be disturbed by muscle fatigue, it recently also has been shown to be improved, under normal ankle neuromuscular state, through the use of an artificial tongue-placed tactile biofeedback. The underlying principle of this biofeedback consisted of supplying individuals with supplementary information about the position of their matching ankle position relative to their reference ankle position through electrotactile stimulation of the tongue. Within this context, the purpose of the present experiment was to investigate whether this biofeedback could mitigate the deleterious effect of muscle fatigue on joint position sense at the ankle. To address this objective, sixteen young healthy university students were asked to perform an active ankle-matching task in two conditions of No-fatigue and Fatigue of the ankle muscles and two conditions of No-biofeedback and Biofeedback. Measures of the overall accuracy and the variability of the positioning were determined using the absolute error and the variable error, respectively. Results showed that the availability of the biofeedback allowed the subjects to suppress the deleterious effects of muscle fatigue on joint position sense at the ankle. In the context of sensory re-weighting process, these findings suggested that the central nervous system was able to integrate and increase the relative contribution of the artificial tongue-placed tactile biofeedback to compensate for a proprioceptive degradation at the ankle.


Sensory re-weighting Biofeedback Proprioception Muscle fatigue Tongue display unit Ankle 



The authors are indebted to Professor Paul Bach-y-Rita for introducing us to the Tongue Display Unit and for discussions about sensory substitution. Paul has been for us more than a partner or a supervisor: he was a master inspiring numerous new fields of research in many domains of neuroscience, biomedical engineering and physical rehabilitation. The authors would like to thank subject volunteers. Special thanks also are extended to Damien Flammarion and Sylvain Maubleu for technical assistance, Benjamin Bouvier for his help in data collection, Dr. Vince and Zora B. for various contributions. This research was supported by the Fondation Garches and the company IDS.


  1. Allen TJ, Proske U (2006) Effect of muscle fatigue on the sense of limb position and movement. Exp Brain Res 170:30–38PubMedCrossRefGoogle Scholar
  2. Bach-y-Rita P, Kercel SW (2003) Sensory substitution and the human-machine interface. Trends Cogn Sci 7:541–546PubMedCrossRefGoogle Scholar
  3. Bach-y-Rita P, Kaczmarek KA, Tyler ME, Garcia-Lara J (1998) Form perception with a 49-point electrotactile stimulus array on the tongue. J Rehabil Res Dev 35:427–430PubMedGoogle Scholar
  4. Björklund M, Crenshaw AG, Djupsjöbacka M, Johansson H (2000) Position sense acuity is diminished following repetitive low-intensity work to fatigue in a simulated occupational setting. Eur J Appl Physiol 81:361–367PubMedCrossRefGoogle Scholar
  5. Borg G (1990) Psychological scaling with applications in physical work and the perception of exertion. Scand J Work Environ Health 16:55–58PubMedGoogle Scholar
  6. Bressel E, Larsen BT, McNair PJ, Cronin J (2004) Ankle joint proprioception and passive mechanical properties of the calf muscles after an Achilles tendon rupture: a comparison with matched controls. Clin Biomech 19:284–291CrossRefGoogle Scholar
  7. 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 771:251–258PubMedCrossRefGoogle Scholar
  8. Burke D, Gandevia SC, Macefield G (1998) Responses to passive movement of receptors in joint, skin and muscle of the human hand. J Physiol 402:347–361Google Scholar
  9. Essick GK, Chopra A, Guest S, McGlone F (2003) Lingual tactile acuity, taste perception, and the density and diameter of fungiform papillae in female subjects. Physiol Behav 80:289–302PubMedCrossRefGoogle Scholar
  10. 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 34:117–122PubMedGoogle Scholar
  11. Fu AS, Hui-Chan CW (2005) Ankle joint proprioception and postural control in basketball players with bilateral ankle sprains. Am J Sports Med 33:1174–1182PubMedCrossRefGoogle Scholar
  12. Halasi T, Kynsburg A, Tallay A, Berkes I (2005) Changes in joint position sense after surgically treated chronic lateral ankle instability. Br J Sports Med 39:818–824PubMedCrossRefGoogle Scholar
  13. Horak FB, Macpherson JM (1996) Postural orientation and equilibrium. In: Shepard J, Rowell L (eds), Handbook of physiology, exercise: regulation and integration of multiple systems. Oxford University Press, New York, sect. 2, pp 255–292Google Scholar
  14. Lattanzio PJ, Petrella RJ, Sproule JR, Fowler PJ (1997) Effects of fatigue on knee proprioception. Clin J Sport Med 7:22–27PubMedCrossRefGoogle Scholar
  15. Ledin T, Fransson PA, Magnusson M (2004) Effects of postural disturbances with fatigued triceps surae muscles or with 20% additional body weight. Gait Posture 19:184–193PubMedCrossRefGoogle Scholar
  16. Lee HM, Liau JJ, Cheng CK, Tan CM, Shih JT (2003) Evaluation of shoulder proprioception following muscle fatigue. Clin Biomech 18:843–847CrossRefGoogle Scholar
  17. Madhavan S, Shields RK (2005) Influence of age on dynamic position sense: evidence using a sequential movement task. Exp Brain Res 164:18–28PubMedCrossRefGoogle Scholar
  18. Oie KS, Kiemel T, Jeka JJ (2002) Multisensory fusion: simultaneous re-weighting of vision and touch for the control of human posture brain Res Cogn Brain Res 14:164–176PubMedCrossRefGoogle Scholar
  19. Payne KA, Berg K, Latin RW (1997) Ankle injuries and ankle strength, flexibility, and proprioception in college basketball players. J Athl Train 32:221–225PubMedGoogle Scholar
  20. Picard C, Olivier A (1983) Sensory cortical tongue representation in man. J Neurosurg 59:781–789PubMedCrossRefGoogle Scholar
  21. Sampaio E, Maris S, Bach-y-Rita P (2001) Brain plasticity: ‘visual’ acuity of blind persons via the tongue. Brain Res 908:204–207PubMedCrossRefGoogle Scholar
  22. Schmidt RA (1988) Motor control and learning, 2nd edn. Human Kinetics, ChampaignGoogle Scholar
  23. Simoneau GG, Derr JA, Ulbrecht JS, Becker MB, Cavanagh PR (1996) Diabetic sensory neuropathy effect on ankle joint movement perception. Arch Phys Med Rehabil 77:453–460PubMedCrossRefGoogle Scholar
  24. Skinner HB, Wyatt MP, Hodgdon JA, Conard DW, Barrack RL (1986) Effect of fatigue on joint position sense of the knee. J Orthop Res 4:112–118PubMedCrossRefGoogle Scholar
  25. Taimela S, Kankaanpää M, Luoto S (1999) The effect of lumbar fatigue on the ability to sense a change in lumbar position. Spine 13:1322–1327CrossRefGoogle Scholar
  26. Trulsson M, Essick GK (1997) Low-threshold mechanoreceptive afferents in the human lingual nerve. J Neurophysiol 77:737–748PubMedGoogle Scholar
  27. van Boven RW, Johnson KO (1994) The limit of tactile spatial resolution in humans: grating orientation discrimination at the lips, tongue, and finger. Neurology 44:2361–2366PubMedGoogle Scholar
  28. van den Bosch CG, Gilsing MG, Lee SG, Richardson JK, Ashton-Miller JA (1995) Peripheral neuropathy effect on ankle inversion and eversion detection thresholds. Arch Phys Med Rehabil 76:850–856PubMedCrossRefGoogle Scholar
  29. van Deursen RW, Sanchez MM, Ulbrecht JS, Cavanagh PR (1998) The role of muscle spindles in ankle movement perception in human subjects with diabetic neuropathy. Exp Brain Res 120:1–8PubMedCrossRefGoogle Scholar
  30. Verschueren SM, Brumagne S, Swinnen SP, Cordo PJ (2002) The effect of aging on dynamic position sense at the ankle. Behav Brain Res 136:593–603PubMedCrossRefGoogle Scholar
  31. Voight ML, Hardin JA, Blackburn TA, Tippett S, Canner GC (1996) The effects of muscle fatigue on and the relationship of arm dominance to shoulder proprioception. J Orthop Sports Phys Ther 23:348–353PubMedGoogle Scholar
  32. Vuillerme N, Danion F, Forestier N, Nougier V (2002a) Postural sway under muscle vibration and muscle fatigue in humans. Neurosci Lett 333:131–135PubMedCrossRefGoogle Scholar
  33. Vuillerme N, Forestier N, Nougier V (2002b) Attentional demands and postural sway: the effect of the calf muscles fatigue. Med Sci Sports Exerc 34:1607–1612Google Scholar
  34. Vuillerme N, Nougier V (2003) Effect of light finger touch on postural sway after lower-limb muscular fatigue. Arch Phys Med Rehabil 84:1560–1563PubMedCrossRefGoogle Scholar
  35. Vuillerme N, Pinsault N, Vaillant J (2005a) Postural control during quiet standing following cervical muscular fatigue: effects of changes in sensory inputs. Neurosci Lett 378:135–139PubMedCrossRefGoogle Scholar
  36. Vuillerme N, Pinsault N, Virone G, Vaillant J (2005b) Effects of cervical muscular fatigue on cervicocephalic joint position sense. Expansion scientifique française. Paris, pp 48–52Google Scholar
  37. Vuillerme N, Burdet C, Isableu B, Demetz S (2006a) The magnitude of the effect of calf muscles fatigue on postural control during bipedal quiet standing with vision depends on the eye-visual target distance. Gait Posture 24:169–172PubMedCrossRefGoogle Scholar
  38. Vuillerme N, Chenu O, Demongeot J, Payan Y (2006b) Improving human ankle joint position sense using an artificial tongue-placed tactile biofeedback. Neurosci Lett 405:19–23PubMedCrossRefGoogle Scholar
  39. Vuillerme N, Chenu O, Fleury J, Demongeot J, Payan Y (2006c) Optimizing the use of an artificial tongue-placed tactile biofeedback for improving ankle joint position sense in humans. In: 28th annual international conference of the IEEE engineering in medicine and biology society (EMBS), New York, pp. 6029–6032Google Scholar
  40. Vuillerme N, Demetz S (2007) Do ankle foot orthoses modify postural control during bipedal quiet standing following a localized fatigue at the ankle muscles? Int J Sports Med 28:243–246PubMedCrossRefGoogle Scholar
  41. Vuillerme N, Chenu O, Demongeot J, Payan Y (2007a) Controlling posture using a plantar pressure-based, tongue-placed tactile biofeedback system. Exp Brain Res 179:409–414PubMedCrossRefGoogle Scholar
  42. Vuillerme N, Chenu O, Pinsault N, Boisgontier M, Demongeot J, Payan Y (2007b) Inter-individual variability in sensory weighting of a plantar pressure-based, tongue-placed tactile biofeedback for controlling posture. Neurosci Lett 421:173–177PubMedCrossRefGoogle Scholar
  43. Vuillerme N, Pinsault N, Chenu O, Boisgontier M, Demongeot J, Payan Y (2007c) How a plantar pressure-based, tongue-placed tactile biofeedback modifies postural control mechanisms during quiet standing. Exp Brain Res (doi: 10.1007/s00221-007-0953-9)
  44. Walsh LD, Hesse CW, Morgan DL, Proske U (2004) Human forearm position sense after fatigue elbow flexor muscle. J Physiol 558:705–715PubMedCrossRefGoogle Scholar
  45. Winter JA, Allen TJ, Proske U (2005) Muscle spindle signals combine with the sense of effort to indicate limb position. J Physiol 568:1035–1046PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Nicolas Vuillerme
    • 1
  • Matthieu Boisgontier
    • 1
  • Olivier Chenu
    • 1
  • Jacques Demongeot
    • 1
  • Yohan Payan
    • 1
  1. 1.Laboratoire TIMC-IMAG, UMR UJF CNRS 5525Faculté de MédecineLa Tronche CédexFrance

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