Balance control mechanisms do not benefit from successive stimulation of different sensory systems

Autoři: Jean-Philippe Cyr aff001;  Noémie Anctil aff001;  Martin Simoneau aff001
Působiště autorů: Département de kinésiologie, Faculté de médecine, Université Laval, Québec, Québec, Canada aff001;  Centre interdisciplinaire de recherche en réadaptation et intégration sociale (CIRRIS) du CIUSSS de la Capitale Nationale, Québec, Québec, Canada aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


In humans, to reduce deviations from a perfect upright position, information from various sensory cues is combined and continuously weighted based on its reliability. Combining noisy sensory information to produce a coherent and accurate estimate of body sway is a central problem in human balance control. In this study, we first compared the ability of the sensorimotor control mechanisms to deal with altered ankle proprioception or vestibular information (i.e., the single sensory condition). Then, we evaluated whether successive stimulation of difference sensory systems (e.g., Achilles tendon vibration followed by electrical vestibular stimulation, or vice versa) produced a greater alteration of balance control (i.e., the mix sensory condition). Electrical vestibular stimulation (head turned ~90°) and Achilles tendon vibration induced backward body sways. We calculated the root mean square value of the scalar distance between the center of pressure and the center of gravity as well as the time needed to regain balance (i.e., stabilization time). Furthermore, the peak ground reaction force along the anteroposterior axis, immediately following stimulation offset, was determined to compare the balance destabilization across the different conditions. In single conditions, during vestibular or Achilles tendon vibration, no difference in balance control was observed. When sensory information returned to normal, balance control was worse following Achilles tendon vibration. Compared to that of the single sensory condition, successive stimulation of different sensory systems (i.e., mix conditions) increased stabilization time. Overall, the present results reveal that single and successive sensory stimulation challenges the sensorimotor control mechanisms differently.

Klíčová slova:

Ankles – Functional electrical stimulation – Proprioception – Sensory cues – Sensory perception – Sensory systems – Tendons – Vibration


1. Bronstein AM, Hood JD. The cervico-ocular reflex in normal subjects and patients with absent vestibular function. Brain Res. 1986;373(1–2):399–408. Epub 1986/05/14. doi: 10.1016/0006-8993(86)90355-0 3487371.

2. Kavounoudias A, Gilhodes JC, Roll R, Roll JP. From balance regulation to body orientation: two goals for muscle proprioceptive information processing? Exp Brain Res. 1999;124(1):80–8. Epub 1999/02/03. doi: 10.1007/s002210050602 9928792.

3. Magnusson M, Enbom H, Johansson R, Wiklund J. Significance of pressor input from the human feet in lateral postural control. The effect of hypothermia on galvanically induced body-sway. Acta Otolaryngol. 1990;110(5–6):321–7. Epub 1990/11/01. doi: 10.3109/00016489009107450 2284906.

4. Bronstein AM. Suppression of visually evoked postural responses. Exp Brain Res. 1986;63(3):655–8. Epub 1986/01/01. doi: 10.1007/bf00237488 3489640.

5. Maurer C, Mergner T, Peterka RJ. Multisensory control of human upright stance. Exp Brain Res. 2006;171(2):231–50. Epub 2005/11/25. doi: 10.1007/s00221-005-0256-y 16307252.

6. Oie KS, Kiemel T, Jeka JJ. Multisensory fusion: simultaneous re-weighting of vision and touch for the control of human posture. Brain Res Cogn Brain Res. 2002;14(1):164–76. Epub 2002/06/14. doi: 10.1016/s0926-6410(02)00071-x 12063140.

7. Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol. 2002;88(3):1097–118. Epub 2002/09/03. doi: 10.1152/jn.2002.88.3.1097 12205132.

8. Fitzpatrick RC, Day BL. Probing the human vestibular system with galvanic stimulation. J Appl Physiol (1985). 2004;96(6):2301–16. Epub 2004/05/11. doi: 10.1152/japplphysiol.00008.2004 15133017.

9. Goldberg JM, Smith CE, Fernandez C. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J Neurophysiol. 1984;51(6):1236–56. Epub 1984/06/01. doi: 10.1152/jn.1984.51.6.1236 6737029.

10. Burke D, Hagbarth KE, Lofstedt L, Wallin BG. The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol. 1976;261(3):673–93. Epub 1976/10/01. doi: 10.1113/jphysiol.1976.sp011580 135840; PubMed Central PMCID: PMC1309166.

11. Eklund G. General features of vibration-induced effects on balance. Ups J Med Sci. 1972;77(2):112–24. Epub 1972/01/01. doi: 10.1517/03009734000000016 4262735.

12. Ferre ER, Bottini G, Haggard P. Vestibular modulation of somatosensory perception. Eur J Neurosci. 2011;34(8):1337–44. doi: 10.1111/j.1460-9568.2011.07859.x 21978189.

13. Ferre ER, Day BL, Bottini G, Haggard P. How the vestibular system interacts with somatosensory perception: a sham-controlled study with galvanic vestibular stimulation. Neurosci Lett. 2013;550:35–40. Epub 2013/07/06. doi: 10.1016/j.neulet.2013.06.046 23827220; PubMed Central PMCID: PMC3988931.

14. Hlavacka F, Krizkova M, Horak FB. Modification of human postural response to leg muscle vibration by electrical vestibular stimulation. Neurosci Lett. 1995;189(1):9–12. Epub 1995/04/07. 030439409511436Z [pii]. doi: 10.1016/0304-3940(95)11436-z 7603629.

15. Bottini G, Sterzi R, Paulesu E, Vallar G, Cappa SF, Erminio F, et al. Identification of the central vestibular projections in man: a positron emission tomography activation study. Exp Brain Res. 1994;99(1):164–9. Epub 1994/01/01. doi: 10.1007/bf00241421 7925790.

16. Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A, Lempert T, et al. Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage. 2002;17(3):1384–93. Epub 2002/11/05. S1053811902912413 [pii]. doi: 10.1006/nimg.2002.1241 12414278.

17. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M. Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol. 2001;85(2):886–99. Epub 2001/02/13. doi: 10.1152/jn.2001.85.2.886 11160520.

18. Emri M, Kisely M, Lengyel Z, Balkay L, Marian T, Miko L, et al. Cortical projection of peripheral vestibular signaling. J Neurophysiol. 2003;89(5):2639–46. Epub 2003/05/13. doi: 10.1152/jn.00599.2002 12740408.

19. van der Kooij H, Peterka RJ. Non-linear stimulus-response behavior of the human stance control system is predicted by optimization of a system with sensory and motor noise. J Comput Neurosci. 2011;30(3):759–78. Epub 2010/12/17. doi: 10.1007/s10827-010-0291-y 21161357; PubMed Central PMCID: PMC3108015.

20. Horak FB, Dickstein R, Peterka RJ. Diabetic neuropathy and surface sway-referencing disrupt somatosensory information for postural stability in stance. Somatosens Mot Res. 2002;19(4):316–26. Epub 2003/02/20. doi: 10.1080/0899022021000037782 12590833.

21. Diener HC, Dichgans J, Guschlbauer B, Mau H. The significance of proprioception on postural stabilization as assessed by ischemia. Brain Res. 1984;296(1):103–9. Epub 1984/03/26. doi: 10.1016/0006-8993(84)90515-8 6713202.

22. Lord SR, Clark RD, Webster IW. Postural stability and associated physiological factors in a population of aged persons. J Gerontol. 1991;46(3):M69–76. Epub 1991/05/01. doi: 10.1093/geronj/46.3.m69 2030269.

23. Peterka RJ, Benolken MS. Role of somatosensory and vestibular cues in attenuating visually induced human postural sway. Exp Brain Res. 1995;105(1):101–10. Epub 1995/01/01. doi: 10.1007/bf00242186 7589307.

24. Simoneau GG, Leibowitz HW, Ulbrecht JS, Tyrrell RA, Cavanagh PR. The effects of visual factors and head orientation on postural steadiness in women 55 to 70 years of age. J Gerontol. 1992;47(5):M151–8. Epub 1992/09/01. doi: 10.1093/geronj/47.5.m151 1512430.

25. Simoneau GG, Ulbrecht JS, Derr JA, Cavanagh PR. Role of somatosensory input in the control of human posture. Gait Posture. 1995;3(3):115–22. doi: 10.1016/0966-6362(95)99061-o

26. Caudron S, Nougier V, Guerraz M. Postural challenge and adaptation to vibration-induced disturbances. Exp Brain Res. 2010;202(4):935–41. Epub 2010/03/03. doi: 10.1007/s00221-010-2194-6 20195847.

27. Holmberg J, Karlberg M, Fransson PA, Magnusson M. Phobic postural vertigo: body sway during vibratory proprioceptive stimulation. Neuroreport. 2003;14(7):1007–11. Epub 2003/06/13. doi: 10.1097/01.wnr.0000070191.28954.a5 12802192.

28. Fransson PA, Gomez S, Patel M, Johansson L. Changes in multi-segmented body movements and EMG activity while standing on firm and foam support surfaces. Eur J Appl Physiol. 2007;101(1):81–9. Epub 2007/05/16. doi: 10.1007/s00421-007-0476-x 17503068.

29. Lund S, Broberg C. Effects of different head positions on postural sway in man induced by a reproducible vestibular error signal. Acta Physiol Scand. 1983;117(2):307–9. Epub 1983/02/01. doi: 10.1111/j.1748-1716.1983.tb07212.x 6603098.

30. Cathers I, Day BL, Fitzpatrick RC. Otolith and canal reflexes in human standing. J Physiol. 2005;563(Pt 1):229–34. Epub 2004/12/25. doi: 10.1113/jphysiol.2004.079525 15618274; PubMed Central PMCID: PMC1665570.

31. Elftman H. Forces and energy changes in the leg during walking. Am J Physiol Content. 1939;125(2):339–56. doi: 10.1152/ajplegacy.1939.125.2.339

32. Winter DA. Biomechanics of Human Movement. Toronto: John Wiley & Sons; 1979.

33. King DL, Zatsiorsky VM. Extracting gravity line displacement from stabilographic recordings. Gait Posture. 1997;6(1):27–38. doi: 10.1016/s0966-6362(96)01101-0

34. Zatsiorsky VM, King DL. An algorithm for determining gravity line location from posturographic recordings. J Biomech. 1998;31(2):161–4. doi: 10.1016/s0021-9290(97)00116-4 9593210.

35. Roll JP, Vedel JP. Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res. 1982;47(2):177–90. Epub 1982/01/01. doi: 10.1007/bf00239377 6214420.

36. Simoneau M, Mercier P, Blouin J, Allard P, Teasdale N. Altered sensory-weighting mechanisms is observed in adolescents with idiopathic scoliosis. BMC Neurosci. 2006;7(1):68. Epub 2006/10/21. doi: 10.1186/1471-2202-7-68 17052338; PubMed Central PMCID: PMC1633738.

37. Teasdale N, Simoneau M. Attentional demands for postural control: the effects of aging and sensory reintegration. Gait Posture. 2001;14(3):203–10. Epub 2001/10/16. doi: 10.1016/s0966-6362(01)00134-5 11600323.

38. Kim J, Curthoys IS. Responses of primary vestibular neurons to galvanic vestibular stimulation (GVS) in the anaesthetised guinea pig. Brain Res Bull. 2004;64(3):265–71. doi: 10.1016/j.brainresbull.2004.07.008 15464864.

39. Day BL, Marsden JF, Ramsay E, Mian OS, Fitzpatrick RC. Non-linear vector summation of left and right vestibular signals for human balance. J Physiol. 2010;588(Pt 4):671–82. Epub 2009/12/23. doi: 10.1113/jphysiol.2009.181768 20026614; PubMed Central PMCID: PMC2828139.

40. Mian OS, Dakin CJ, Blouin JS, Fitzpatrick RC, Day BL. Lack of otolith involvement in balance responses evoked by mastoid electrical stimulation. J Physiol. 2010;588(Pt 22):4441–51. Epub 2010/09/22. doi: 10.1113/jphysiol.2010.195222 20855437; PubMed Central PMCID: PMC3008850.

41. Masani K, Vette AH, Kouzaki M, Kanehisa H, Fukunaga T, Popovic MR. Larger center of pressure minus center of gravity in the elderly induces larger body acceleration during quiet standing. Neurosci Lett. 2007;422(3):202–6. Epub 2007/07/06. doi: 10.1016/j.neulet.2007.06.019 17611029.

42. Winter DA. Human balance and posture control during standing and walking. Gait Posture. 1995;3(4):193–214. doi: 10.1016/0966-6362(96)82849-9

43. Tjernstrom F, Fransson PA, Hafstrom A, Magnusson M. Adaptation of postural control to perturbations—a process that initiates long-term motor memory. Gait Posture. 2002;15(1):75–82. Epub 2002/01/26. doi: 10.1016/s0966-6362(01)00175-8 11809583.

44. Ernst MO, Banks MS. Humans integrate visual and haptic information in a statistically optimal fashion. Nature. 2002;415(6870):429–33. Epub 2002/01/25. doi: 10.1038/415429a 11807554.

45. Cullen KE. Physiology of central pathways. Handb Clin Neurol. 2016;137:17–40. Epub 2016/09/18. doi: 10.1016/B978-0-444-63437-5.00002-9 27638060.

46. Guerraz M, Day BL. Expectation and the vestibular control of balance. J Cogn Neurosci. 2005;17(3):463–9. Epub 2005/04/09. doi: 10.1162/0898929053279540 15814005.

47. Nashner LM. Adapting reflexes controlling the human posture. Exp Brain Res. 1976;26(1):59–72. Epub 1976/08/27. doi: 10.1007/bf00235249 964327.

48. Taube W, Schubert M, Gruber M, Beck S, Faist M, Gollhofer A. Direct corticospinal pathways contribute to neuromuscular control of perturbed stance. J Appl Physiol (1985). 2006;101(2):420–9. Epub 2006/04/08. doi: 10.1152/japplphysiol.01447.2005 16601305.

49. Tokuno CD, Taube W, Cresswell AG. An enhanced level of motor cortical excitability during the control of human standing. Acta Physiol (Oxf). 2009;195(3):385–95. Epub 2008/09/09. doi: 10.1111/j.1748-1716.2008.01898.x 18774948.

50. Golanov EV, Christensen JR, Reis DJ. Neurons of a limited subthalamic area mediate elevations in cortical cerebral blood flow evoked by hypoxia and excitation of neurons of the rostral ventrolateral medulla. J Neurosci. 2001;21(11):4032–41. Epub 2001/05/23. doi: 10.1523/JNEUROSCI.21-11-04032.2001 11356890.

51. Stelmach GE, Teasdale N, Di Fabio RP, Phillips J. Age related decline in postural control mechanisms. Int J Aging Hum Dev. 1989;29(3):205–23. Epub 1989/01/01. doi: 10.2190/KKP0-W3Q5-6RDN-RXYT 2634030.

52. Roll JP, Vedel JP, Ribot E. Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res. 1989;76(1):213–22. doi: 10.1007/bf00253639 2753103.

53. Proske U, Gandevia SC. The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev. 2012;92(4):1651–97. Epub 2012/10/18. doi: 10.1152/physrev.00048.2011 23073629.

54. Ivanenko YP, Talis VL, Kazennikov OV. Support stability influences postural responses to muscle vibration in humans. Eur J Neurosci. 1999;11(2):647–54. Epub 1999/03/03. doi: 10.1046/j.1460-9568.1999.00471.x 10051765.

55. Grasso R, Ivanenko YP, McIntyre J, Viaud-Delmon I, Berthoz A. Spatial, not temporal cues drive predictive orienting movements during navigation: a virtual reality study. Neuroreport. 2000;11(4):775–8. Epub 2000/04/11. doi: 10.1097/00001756-200003200-00024 10757518.

56. Popov KE, Kozhina GV, Smetanin BN, Shlikov VY. Postural responses to combined vestibular and hip proprioceptive stimulation in man. Eur J Neurosci. 1999;11(9):3307–11. Epub 1999/10/06. doi: 10.1046/j.1460-9568.1999.00733.x 10510195.

57. Lackner JR, DiZio PA. Aspects of body self-calibration. Trends Cogn Sci. 2000;4(7):279–88. Epub 2000/06/22. doi: 10.1016/s1364-6613(00)01493-5 10859572.

58. Adamcova N, Hlavacka F. Modification of human postural responses to soleus muscle vibration by rotation of visual scene. Gait Posture. 2007;25(1):99–105. doi: 10.1016/j.gaitpost.2006.01.008 16621566

59. Assländer L, Peterka RJ. Sensory reweighting dynamics following removal and addition of visual and proprioceptive cues. J Neurophysiol. 2016;116(2):272–85. doi: 10.1152/jn.01145.2015 27075544

60. Inglis JT, Shupert CL, Hlavacka F, Horak FB. Effect of galvanic vestibular stimulation on human postural responses during support surface translations. J Neurophysiol. 1995;73(2):896–901. Epub 1995/02/01. doi: 10.1152/jn.1995.73.2.896 7760147.

61. Fetsch CR, DeAngelis GC, Angelaki DE. Bridging the gap between theories of sensory cue integration and the physiology of multisensory neurons. Nat Rev Neurosci. 2013;14(6):429–42. doi: 10.1038/nrn3503 23686172; PubMed Central PMCID: PMC3820118.

62. Meredith MA, Stein BE. Interactions among converging sensory inputs in the superior colliculus. Science. 1983;221(4608):389–91. Epub 1983/07/22. doi: 10.1126/science.6867718 6867718.

63. Meredith MA, Stein BE. Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J Neurophysiol. 1986;56(3):640–62. Epub 1986/09/01. doi: 10.1152/jn.1986.56.3.640 3537225.

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