Advertisement

Experimental Brain Research

, Volume 212, Issue 1, pp 33–46 | Cite as

Differential integration of visual and kinaesthetic signals to upright stance

  • Brice IsableuEmail author
  • Benoît Fourre
  • Nicolas Vuillerme
  • Guillaume Giraudet
  • Michel-Ange Amorim
Research Article

Abstract

The present experiment was designed to assess the effect of active (deliberate) maintenance of a small forward (FL) or backward body lean (BL) (about 2° ankle flexion) with respect to the spontaneous direction of balance (or neutral posture, N) on postural balance. We questioned whether BL and FL stances, which impose a volitional proprioceptive control of the body-on-support angle, could efficiently reduce mediolateral displacements of the centre of pressure (CoP) induced by the visual motion of a room and darkness. Subjects (n = 15) were asked to stand upright quietly feet together while confronted to a large visual scene rolling to 10° on either side in peripheral vision (and surrounding vertical visual references in central vision) at 0.05 Hz. CoP displacements were recorded using a force platform. Analysis of medio-lateral CoP root-mean square showed that the effect of the moving room depends on the subject’s postural stability performance in the eyes open N stance condition. Two significant postural behaviours emerged. (1) The most stable subjects (G1) were not affected by the conditions of altered vision, but swayed more in BL stance than in the N stance. (2) The unstable subjects (G2) exhibited (i) larger CoP displacements in altered visual conditions and a greater coupling of the CoP with the motion of the visual scene, (ii) enhanced visual dependency with postural leaning, and (iii) decreased CoP displacements when leaning forward in the eyes open motionless scene. Interestingly, the visual quotient positively correlated with the proprioceptive quotient, indicating that the more the subjects relied heavily on the visual frame of reference (FOR) the more they were influenced by body leaning. This result suggested hence a lesser ability to use efficiently body-ground proprioceptive cues. On the whole, the present findings indicate that body leaning could provide a useful mean to assess the subject’s ability to use body-ground proprioceptive cues not only to improve postural stability during eyes opening (especially during forward leaning), but also as a mean to disclose subjects’ visual dependency and their associated difficulties to shift from visual to proprioceptive-based FOR.

Keywords

Proprioception Vision Postural control Frames of reference Interindividual variability Human 

Notes

Acknowledgments

The authors would like to thank the students at the University Paris-Sud, UFR STAPS who volunteered to serve as participants in this study. This research was supported by a grant from the Centre National de la Recherche Scientifique, île de France.

References

  1. Anand V, Buckley J, Scally A, Elliott DB (2002) The effect of refractive blur on postural stability. Ophthalmic Physiol Opt 22:528–534PubMedGoogle Scholar
  2. Anastasopoulos D, Bronstein AM (1999) A case of thalamic syndrome: somatosensory influences on visual orientation. J Neurol Neurosurg Psychiatr 67:390–394PubMedGoogle Scholar
  3. Anastasopoulos D, Bronstein A, Haslwanter T, Fetter M, Dichgans J (1999) The role of somatosensory input for the perception of verticality. Ann NY Acad Sci 871:379–383PubMedGoogle Scholar
  4. Avillac M, Deneve S, Olivier E, Pouget A, Duhamel JR (2005) Reference frames for representing visual and tactile locations in parietal cortex. Nat Neurosci 8:941–949PubMedGoogle Scholar
  5. Babler TG, Ebenholtz SM (1989) Effects of peripheral circular contours on dynamic spatial orientation. Percept Psychophys 45:307–314PubMedGoogle Scholar
  6. Barbieri G, Gissot AS, Fouque F, Casillas JM, Pozzo T, Perennou D (2008) Does proprioception contribute to the sense of verticality? Exp Brain Res 185:545–552PubMedGoogle Scholar
  7. Bernard-Demanze L, Burdet C, Berger L, Rougier P (2004) Recalibration of somaesthetic plantar information in the control of undisturbed upright stance maintenance. J Integr Neurosci 3:433–451PubMedGoogle Scholar
  8. Bernard-Demanze L, Vuillerme N, Ferry M, Berger L (2009) Can tactile plantar stimulation improve postural control of persons with superficial plantar sensory deficit? Aging Clin Exp Res 21:62–68PubMedGoogle Scholar
  9. Bernardin D, Isableu B, Fourcade P, Bardy BG (2005) Differential exploitation of the inertia tensor in multi-joint arm reaching. Exp Brain Res 167:487–495PubMedGoogle Scholar
  10. Berthoz A (1991) Reference frames for the perception and control of movement. In: Paillard J (ed) Brain and space. Oxford University Press, Oxford, pp 81–110Google Scholar
  11. Blaszczyk JW, Hansen PD, Lowe DL (1993) Postural sway and perception of the upright stance stability borders. Perception 22:1333–1341PubMedGoogle Scholar
  12. Bonnet CT, Faugloire E, Riley MA, Bardy BG, Stoffregen TA (2006) Motion sickness preceded by unstable displacements of the center of pressure. Hum Mov Sci 25:800–820PubMedGoogle Scholar
  13. Carver S, Kiemel T, Van der KH, Jeka JJ (2005) Comparing internal models of the dynamics of the visual environment. Biol Cybern 92:147–163PubMedGoogle Scholar
  14. Carver S, Kiemel T, Jeka JJ (2006) Modeling the dynamics of sensory reweighting. Biol Cybern 95:123–134PubMedGoogle Scholar
  15. Chiari L, Bertani A, Cappello A (2000) Classification of visual strategies in human postural control by stochastic parameters. Hum Mov Sci 19:817–842Google Scholar
  16. Chiari L, Rocchi L, Cappello A (2002) Stabilometric parameters are affected by anthropometry and foot placement. Clin Biomech 17:666–677Google Scholar
  17. Claeys K, Brumagne S, Dankaerts W, Kiers H, Janssens L (2011) Decreased variability in postural control strategies in young people with non-specific low back pain is associated with altered proprioceptive reweighting. Eur J Appl Physiol 111:115–123PubMedGoogle Scholar
  18. Collins JJ, De Luca CJ (1995) The effects of visual input on open-loop and closed-loop postural control mechanisms. Exp Brain Res 103:151–163PubMedGoogle Scholar
  19. Deneve S, Pouget A (2004) Bayesian multisensory integration and cross-modal spatial links. J Physiol Paris 98:249–258PubMedGoogle Scholar
  20. Dietz V (1998) Evidence for a load receptor contribution to the control of posture and locomotion. Neurosci Biobehav Rev 22:495–499PubMedGoogle Scholar
  21. Dietz V, Duysens J (2000) Significance of load receptor input during locomotion: a review. Gait Posture 11:102–110PubMedGoogle Scholar
  22. Dokka K, Kenyon RV, Keshner EA (2009) Influence of visual scene velocity on segmental kinematics during stance. Gait Posture 30:211–216PubMedGoogle Scholar
  23. Dokka K, Kenyon RV, Keshner EA, Kording KP (2010) Self versus environment motion in postural control. PLoS Comput Biol 6:e1000680PubMedGoogle Scholar
  24. Duarte M, Zatsiorsky VM (1999) Patterns of center of pressure migration during prolonged unconstrained standing. Mot Control 3:12–27Google Scholar
  25. Duarte M, Zatsiorsky VM (2002) Effects of body lean and visual information on the equilibrium maintenance during stance. Exp Brain Res 146:60–69PubMedGoogle Scholar
  26. Durbaba R, Taylor A, Ellaway PH, Rawlinson S (2003) The influence of bag2 and chain intrafusal muscle fibers on secondary spindle afferents in the cat. J Physiol 550:263–278PubMedGoogle Scholar
  27. Ebenholtz SM (1977) Determinants of the rod and frame effect: the role of retinal size. Percept Psychophys 22:531–538Google Scholar
  28. Ebenholtz SM, Callan JW (1980) Modulation of the rod and frame effect: retinal angle versus apparent size. Psychol Res 42:327–334Google Scholar
  29. Ehrenfried T, Guerraz M, Thilo KV, Yardley L, Gresty MA (2003) Posture and mental task performance when viewing a moving visual field. Brain Res Cogn Brain Res 17:140–153PubMedGoogle Scholar
  30. Ernst MO, Banks MS (2002) Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415:429–433PubMedGoogle Scholar
  31. Ernst MO, Bulthoff HH (2004) Merging the senses into a robust percept. Trends Cogn Sci 8:162–169PubMedGoogle Scholar
  32. Faugloire E, Bonnet CT, Riley MA, Bardy BG, Stoffregen TA (2007) Motion sickness, body movement, and claustrophobia during passive restraint. Exp Brain Res 177:520–532PubMedGoogle Scholar
  33. Fourre B, Isableu B, Bernardin D, Gueguen M, Giraudet G, Vuillerme N, Pagano C, Amorim MA (2009) The role of body centre of mass on haptic subjective vertical. Neurosci Lett 465:230–234PubMedGoogle Scholar
  34. Gandevia SC, Smith JL, Crawford M, Proske U, Taylor JL (2006) Motor commands contribute to human position sense. J Physiol 571:703–710PubMedGoogle Scholar
  35. Garrett SR, Pagano C, Austin G, Turvey MT (1998) Spatial and physical frames of reference in positioning a limb. Percept Psychophys 60:1206–1215PubMedGoogle Scholar
  36. 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 133:340–348PubMedGoogle Scholar
  37. Guerraz M, Gianna CC, Burchill PM, Gresty MA, Bronstein AM (2001a) Effect of visual surrounding motion on body sway in a three-dimensional environment. Percept Psychophys 63:47–58PubMedGoogle Scholar
  38. Guerraz M, Thilo KV, Bronstein AM, Gresty MA (2001b) Influence of action and expectation on visual control of posture. Brain Res Cogn Brain Res 11:259–266PubMedGoogle Scholar
  39. Hillis JM, Ernst MO, Banks MS, Landy MS (2002) Combining sensory information: mandatory fusion within, but not between, senses. Science 298:1627–1630PubMedGoogle Scholar
  40. Horstmann GA, Dietz V (1990) A basic posture control mechanism: the stabilization of the centre of gravity. Electroencephalogr Clin Neurophysiol 76:165–176PubMedGoogle Scholar
  41. Isableu B, Vuillerme N (2006) Differential integration of kinaesthetic signals to postural control. Exp Brain Res 174:763–768PubMedGoogle Scholar
  42. Isableu B, Ohlmann T, Cremieux J, Amblard B (1997) Selection of spatial frame of reference and postural control variability. Exp Brain Res 114:584–589PubMedGoogle Scholar
  43. Isableu B, Ohlmann T, Cremieux J, Amblard B (2003) Differential approach to strategies of segmental stabilisation in postural control. Exp Brain Res 150:208–221PubMedGoogle Scholar
  44. Isableu B, Rezzoug N, Mallet G, Bernardin D, Gorce P, Pagano CC (2009) Velocity-dependent changes of rotational axes in the non-visual control of unconstrained 3-D arm motions. Neuroscience 164:1632–1647PubMedGoogle Scholar
  45. Isableu B, Ohlmann T, Cremieux J, Vuillerme N, Amblard B, Gresty MA (2010) Individual differences in the ability to identify, select and use appropriate frames of reference for perceptuo-motor control. Neuroscience 169:1199–1215PubMedGoogle Scholar
  46. Kavounoudias A, Roll R, Roll JP (1998) The plantar sole is a dynamometric map for human balance control. Neuroreport 9:3247–3252PubMedGoogle Scholar
  47. Kavounoudias A, Roll R, Roll JP (2001) Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation. J Physiol 532:869–878PubMedGoogle Scholar
  48. Keshner EA, Dhaher Y (2008) Characterizing head motion in three planes during combined visual and base of support disturbances in healthy and visually sensitive subjects. Gait Posture 28:127–134PubMedGoogle Scholar
  49. Keshner EA, Kenyon RV (2000) The influence of an immersive virtual environment on the segmental organization of postural stabilizing responses. J Vestib Res 10:207–219PubMedGoogle Scholar
  50. Keshner EA, Kenyon RV, Dhaher Y (2004) Postural research and rehabilitation in an immersive virtual environment. Conf Proc IEEE Eng Med Biol Soc 7:4862–4865PubMedGoogle Scholar
  51. Kiemel T, Oie KS, Jeka JJ (2002) Multisensory fusion and the stochastic structure of postural sway. Biol Cybern 87:262–277PubMedGoogle Scholar
  52. Kluzik J, Horak FB, Peterka RJ (2005) Differences in preferred reference frames for postural orientation shown by after-effects of stance on an inclined surface. Exp Brain Res 162:474–489PubMedGoogle Scholar
  53. Kluzik J, Peterka RJ, Horak FB (2007) Adaptation of postural orientation to changes in surface inclination. Exp Brain Res 178:1–17PubMedGoogle Scholar
  54. Knill DC, Pouget A (2004) The Bayesian brain: the role of uncertainty in neural coding and computation. Trends Neurosci 27:712–719PubMedGoogle Scholar
  55. Kording KP, Wolpert DM (2004a) Bayesian integration in sensorimotor learning. Nature 427:244–247PubMedGoogle Scholar
  56. Kording KP, Wolpert DM (2004b) The loss function of sensorimotor learning. Proc Natl Acad Sci USA 101:9839–9842PubMedGoogle Scholar
  57. Lacour M, Barthelemy J, Borel L, Magnan J, Xerri C, Chays A, Ouaknine M (1997) Sensory strategies in human postural control before and after unilateral vestibular neurotomy. Exp Brain Res 115:300–310PubMedGoogle Scholar
  58. Lambrey S, Berthoz A (2003) Combination of conflicting visual and non-visual information for estimating actively performed body turns in virtual reality. Int J Psychophysiol 50:101–115PubMedGoogle Scholar
  59. Ledin T, Fransson PA, Magnusson M (2004) Effects of postural disturbances with fatigued triceps surae muscles or with 20% additional body weight. Gait Posture 19:184–193PubMedGoogle Scholar
  60. Massion J (1994) Postural control system. Curr Opin Neurobiol 4:877–887PubMedGoogle Scholar
  61. Massion J, AB Assaiante, Christine ML, Vernazza S (1998) Body orientation and control of coordinated movements in microgravity. Brain Res Rev 28:83–91PubMedGoogle Scholar
  62. Maurer C, Peterka RJ (2005) A new interpretation of spontaneous sway measures based on a simple model of human postural control. J Neurophysiol 93:189–200PubMedGoogle Scholar
  63. Mergner T, Schweigart G, Maurer C, Blumle A (2005) Human postural responses to motion of real and virtual visual environments under different support base conditions. Exp Brain Res 167:535–556PubMedGoogle Scholar
  64. Njiokiktjien CJ, van Parys JA (1976) Romberg’s sign expressed in a quotient. II. Pathology. Agressologie 17:19–23PubMedGoogle Scholar
  65. Ohlmann T (1998) La perception de la verticale. Variabilité interindividuelle dans la dépendance à l’égard des référentiels spatiaux. Université de Paris VIII. Thèse d’état, pp 1–428. Ref type: thesis/dissertationGoogle Scholar
  66. Ohlmann T, Marendaz C (1991) Vicarious processes involved in selection/control of frames of reference and spatial aspects of field dependence-independence. In: Wapner S, Demick J (eds) Field dependence-independence: cognitive style across the life span. L. E. A. Publisher Hillsdale, NJ, pp 105–129Google Scholar
  67. 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 14:164–176PubMedGoogle Scholar
  68. Pagano CC, Turvey MT (1995) The inertia tensor as a basis for the perception of limb orientation. J Exp Psychol Hum Percept Perform 21:1070–1087PubMedGoogle Scholar
  69. Paillard J (1991) Motor and representational framing in space. In: Paillard J (ed) Brain and space. Oxford University Press, Oxford, pp 163–182Google Scholar
  70. Paulus WM, Straube A, Brandt T (1984) Visual stabilization of posture. Physiological stimulus characteristics and clinical aspects. Brain 107:1143–1163PubMedGoogle Scholar
  71. Peterka RJ, Loughlin PJ (2004) Dynamic regulation of sensorimotor integration in human postural control. J Neurophysiol 91:410–423PubMedGoogle Scholar
  72. Pinsault N, Vuillerme N (2009) Test-retest reliability of centre of foot pressure measures to assess postural control during unperturbed stance. Med Eng Phys 31:276–286PubMedGoogle Scholar
  73. Priplata AA, Niemi JB, Harry JD, Lipsitz LA, Collins JJ (2003) Vibrating insoles and balance control in elderly people. Lancet 362:1123–1124PubMedGoogle Scholar
  74. Proske U, Gandevia SC (2009) The kinaesthetic senses. J Physiol 587:4139–4146PubMedGoogle Scholar
  75. Redfern MS, Yardley L, Bronstein AM (2001) Visual influences on balance. J Anxiety Disord 15:81–94PubMedGoogle Scholar
  76. Reuchlin M (1978) Processus vicariants et différences individuelles. J Psychol 2:133–145Google Scholar
  77. Reynolds RF (2010) The ability to voluntarily control sway reflects the difficulty of the standing task. Gait Posture 31:78–81PubMedGoogle Scholar
  78. Riccio GE, Martin EJ, Stoffregen TA (1992) The role of balance dynamics in the active perception of orientation. J Exp Psychol Hum Percept Perform 18:624–644PubMedGoogle Scholar
  79. Rietdyk S, McGlothlin JD, Knezovich MJ (2005) Work experience mitigated age-related differences in balance and mobility during surface accommodation. Clin Biomech 20:1085–1093Google Scholar
  80. Riley MA, Wong S, Mitra S, Turvey MT (1997) Common effects of touch and vision on postural parameters. Exp Brain Res 117:165–170PubMedGoogle Scholar
  81. Roll JP, Roll R (1988) From eye to foot: a proprioceptive chain involved in postural control. In: Amblard B, Berthoz A, Clarac F (eds) Posture and gait: development, adaptation and modulation. Elsevier, Amsterdam, pp 155–164Google Scholar
  82. Rougier P (2001) A forward leaning posture affects more the amplitudes of the centre of pressure displacements than those of the centre of gravity. Ann Readapt Med Phys 44:533–541PubMedGoogle Scholar
  83. Rougier P, Burdet C, Farenc I, Berger L (2001) Backward and forward leaning postures modelled by an fBm framework. Neurosci Res 41:41–50PubMedGoogle Scholar
  84. Schieppati M, Hugon M, Grasso M, Nardone A, Galante M (1994) The limits of equilibrium in young and elderly normal subjects and in parkinsonians. Electroencephalogr Clin Neurophysiol 93:286–298PubMedGoogle Scholar
  85. Simeonov P, Hsiao H (2001) Height, surface firmness, and visual reference effects on balance control. Inj Prev 7(Suppl 1):i50–i53PubMedGoogle Scholar
  86. Sinha T, Maki BE (1996) Effect of forward lean on postural ankle dynamics. IEEE Trans Rehabil Eng 4:348–359PubMedGoogle Scholar
  87. Slaboda JC, Barton JE, Maitin IB, Keshner EA (2009) Visual field dependence influences balance in patients with stroke. Conf Proc IEEE Eng Med Biol Soc 2009:1147–1150PubMedGoogle Scholar
  88. Smith JL, Crawford 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 106:950–958PubMedGoogle Scholar
  89. Stoffregen TA, Riccio GE (1988) An ecological theory of orientation and the vestibular system. Psychol Rev 95:3–14PubMedGoogle Scholar
  90. Stoffregen TA, Smart LJ Jr (1998) Postural instability precedes motion sickness. Brain Res Bull 47:437–448PubMedGoogle Scholar
  91. Stoffregen TA, Hettinger LJ, Haas MW, Roe MM, Smart LJ (2000a) Postural instability and motion sickness in a fixed-based flight simulator. Hum Factors 42:458–469PubMedGoogle Scholar
  92. Stoffregen TA, Pagulayan RJ, Bardy BG, Hettinger LJ (2000b) Modulating postural control to facilitate visual performance. Hum Mov Sci 19:203–220Google Scholar
  93. Streepey JW, Kenyon RV, Keshner EA (2007) Visual motion combined with base of support width reveals variable field dependency in healthy young adults. Exp Brain Res 176:182–187PubMedGoogle Scholar
  94. Suprak DN, Osternig LR, Van DP, Karduna AR (2006) Shoulder joint position sense improves with elevation angle in a novel, unconstrained task. J Orthop Res 24:559–568PubMedGoogle Scholar
  95. Suprak DN, Osternig LR, Van DP, Karduna AR (2007) Shoulder joint position sense improves with external load. J Mot Behav 39:517–525PubMedGoogle Scholar
  96. Thilo KV, Gresty MA (2002) Visual motion stimulation, but not visually induced perception of self-motion, biases the perceived direction of verticality. Brain Res Cogn Brain Res 14:258–263PubMedGoogle Scholar
  97. Vaillant J, Vuillerme N, Janvey A, Louis F, Braujou R, Juvin R, Nougier V (2008) Effect of manipulation of the feet and ankles on postural control in elderly adults. Brain Res Bull 75:18–22PubMedGoogle Scholar
  98. van Parys JA, Njiokiktjien CJ (1976) Romberg’s sign expressed in a quotient. Agressologie 17:95–99PubMedGoogle Scholar
  99. Vuillerme N, Pinsault N (2007) Re-weighting of somatosensory inputs from the foot and the ankle for controlling posture during quiet standing following trunk extensor muscles fatigue. Exp Brain Res 183:323–327PubMedGoogle Scholar
  100. Vuillerme N, Burdet C, Isableu B, Demetz S (2006) 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 24:169–172PubMedGoogle Scholar
  101. Vuillerme N, Chenu O, Demongeot J, Payan Y (2007) Controlling posture using a plantar pressure-based, tongue-placed tactile biofeedback system. Exp Brain Res 179:409–414PubMedGoogle Scholar
  102. Walsh LD, Gandevia SC, Taylor JL (2010) Illusory movements of a phantom hand grade with the duration and magnitude of motor commands. J Physiol 588:1269–1280PubMedGoogle Scholar
  103. Witkin HA, Wapner S (1950) Large oscillating visual displays increase postural instability. Am J Psychol 63:385–392PubMedGoogle Scholar
  104. Zoccolotti P, Antonucci G, Goodenough DR, Pizzamiglio L, Spinelli D (1992) The role of frame size on vertical and horizontal observers in the rod- and-frame illusion. Acta Psychol 79:171–1873Google Scholar
  105. Zoccolotti P, Antonucci G, Daini R, Martelli ML, Spinelli D (1997) Frame-of-reference and hierarchical-organisation effects in the rod-and-frame illusion. Perception 26:1485–1494PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Brice Isableu
    • 1
    • 2
    Email author
  • Benoît Fourre
    • 1
    • 3
  • Nicolas Vuillerme
    • 2
    • 4
  • Guillaume Giraudet
    • 3
    • 5
  • Michel-Ange Amorim
    • 1
    • 6
  1. 1.CIAMS-Motor Control and Perception TeamUniv Paris SudParisFrance
  2. 2.CNRS-UJF-EPHEAGIM (AGeing, Imageing, Modeling) LaboratoryGrenobleFrance
  3. 3.Vision Science DepartmentEssilor International, R and DParisFrance
  4. 4.CIC-IT 805, INSERM/AP-HPHôpital Raymond PoincaréGarchesFrance
  5. 5.Laboratoire de Psychophysique et Perception VisuelleUniv MontréalMontréalCanada
  6. 6.Institut Universitaire de FranceParisFrance

Personalised recommendations