Skip to main content

Advertisement

Log in

Differences in preferred reference frames for postural orientation shown by after-effects of stance on an inclined surface

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

This study reports a postural after-effect of leaning that follows a period of stance on an inclined surface with eyes closed. This leaning after-effect maintained the body-to-surface relationship as if subjects still stood on the incline. We examined the incidence and robustness of the leaning after-effect in 51 healthy subjects. The location of the center of pressure (CoP) under the feet and the alignment of the trunk and legs were measured before, during and after blindfolded subjects stood on a 5° toes-up inclined surface for 2.5 min. When the surface was inclined, all subjects stood with their trunk and legs aligned near to gravity-vertical, similar to the alignment adopted in the pre-incline period. When the surface returned to horizontal in the post-incline period, there was a continuum of postural alignment strategies across subjects. At one extreme, subjects leaned forward, with an average trunk lean near 5°. The leaned posture decayed exponentially toward baseline postural alignment across a period of up to 5 min. At the other extreme, subjects did not lean in the post-incline period, but instead, stayed aligned near upright with respect to gravity. Subjects were highly consistent in their post-incline postural behaviors upon repeated testing over days to months and across different directions of surface inclination. Our results suggest that individuals have well-established, preferred, sensory strategies for controlling postural orientation when vision is not available. Subjects who leaned in the post-incline period appear to depend more on the geometry of the support surface as a reference frame and to rely more on proprioceptive information to extract kinematic relationships, whereas subjects who did not lean appear to depend more on gravity as a reference frame and to rely more on sensory information related to forces and load.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1a–d
Fig. 2a, b
Fig. 3
Fig. 4a, b
Fig. 5a, b
Fig. 6a, b
Fig. 7a–d
Fig. 8
Fig. 9a–c

Similar content being viewed by others

References

  • Anstis S (1995) Aftereffects from jogging. Exp Brain Res 103:476–478

    Article  CAS  PubMed  Google Scholar 

  • Asch SE, Witkin HA (1948) Studies in space orientation. II. Perception of the upright with displaced visual fields and with body tilted. J Exp Psychol 38:455–477

    Google Scholar 

  • Berthoz A (1991) Reference frames for the perception and control of movement. In: Paillard J (ed) Brain and space. Oxford University Press, Oxford, pp 81–111

  • Black FO, Wall C, Nashner LM (1983) Effects of visual and support surface orientation references upon postural control in vestibular deficient subjects. Acta Otolaryngol 95:199–210

    CAS  PubMed  Google Scholar 

  • Brandt T, Dichgans J, Buchele W (1974) Motion habituation: inverted self-motion perception and optokinetic after-nystagmus. Exp Brain Res 21:337–352

    Article  CAS  PubMed  Google Scholar 

  • Bringoux L, Marin L, Nougier V, Barraud PA, Raphel C (2000) Effects of gymnastics expertise on the perception of body orientation in the pitch dimension. J Vestib Res 10:251–258

    CAS  PubMed  Google Scholar 

  • Chiari L, Bertani A, Cappello A (2000) Classification of visual strategies in human postural control by stochastic parameters. Human Mov Sci 19:817–842

    Article  Google Scholar 

  • Cohen B, Matsuo V, Raphan T (1977) Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J Physiol 270:321–344

    CAS  PubMed  Google Scholar 

  • Collins JJ, De Luca CJ (1995) The effects of visual input on open-loop and closed-loop postural control mechanisms. Exp Brain Res 103:151–163

    CAS  PubMed  Google Scholar 

  • Creath R, Kiemel T, Horak F, Jeka JJ (2002) Limited control strategies with the loss of vestibular function. Exp Brain Res 145:323–333

    Article  PubMed  Google Scholar 

  • Cremieux J, Mesure S (1994) Differential sensitivity to static visual cues in the control of postural equilibrium in man. Percept Mot Skills 78:67–74

    CAS  PubMed  Google Scholar 

  • Day BL, Cauquil AS, Bartolomei L, Pastor MA, Lyon IN (1997) Human body-segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. J Physiol 500:661–672

    PubMed  Google Scholar 

  • Dichgans J, Held R, Young LR, Brandt T (1972) Moving visual scenes influence the apparent direction of gravity. Science 178:1217–1219

    CAS  PubMed  Google Scholar 

  • Dickstein R, Shupert CL, Horak FB (2001) Fingertip touch improves postural stability in patients with peripheral neuropathy. Gait Posture 14:238–247

    Article  CAS  PubMed  Google Scholar 

  • Dietz V, Gollhofer A, Kleiber M, Trippel M (1992) Regulation of bipedal stance: dependency on ‘load’ receptors. Exp Brain Res 89:229–231

    Article  CAS  PubMed  Google Scholar 

  • Duarte M, Zatsiorsky VM (1999) Patterns of center of pressure migration during prolonged unconstrained standing. Motor Control 3:12–27

    CAS  PubMed  Google Scholar 

  • Duclos C, Roll R, Kavounoudias A, Roll JP (2004) Long-lasting body leanings following neck muscle isometric contractions. Exp Brain Res 158:58–66

    Article  CAS  PubMed  Google Scholar 

  • Earhart GM, Melvill Jones G, Horak FB, Block EW, Weber KD, Fletcher WA (2001) Forward versus backward walking: transfer of podokinetic adaptation. J Neurophysiol 86:1666–1670

    CAS  PubMed  Google Scholar 

  • Eklund G (1972) General features of vibration-induced effects on balance. Ups J Med Sci 77:112–124

    CAS  PubMed  Google Scholar 

  • Eklund G, Hagbarth KE (1966) Normal variability of tonic vibration reflexes in man. Exp Neurol 16:80–92

    Article  CAS  PubMed  Google Scholar 

  • Fransson P-A, Johansson R, Hafström A, Magnusson M (2000) Methods for evaluation of postural control adaptation. Gait Posture 12:14–24

    Google Scholar 

  • Fransson P-A, Tjernstrom F, Hafström A, Magnusson M, Johansson R (2002) Analysis of short- and long-term effects of adaptation in human postural control. Biol Cybern 86:355–365

    Article  PubMed  Google Scholar 

  • Gibson JJ (1952) The relation between visual and postural determinants of the phenomenal vertical. Psychol Rev 59:370–375

    CAS  PubMed  Google Scholar 

  • Ghafouri M, Thullier F, Gurfinkel VS, Lestienne FG (1998) Muscular after-contraction and ongoing postural reactions in standing and sitting humans. Neurosci Lett 250:61–65

    Google Scholar 

  • Gilhodes JC, Gurfinkel VS, Roll JP (1992) Role of Ia muscle spindle afferents in post-contraction and post-vibration motor effect genesis. Neurosci Lett 135:247–251

    Google Scholar 

  • Golomer E, Cremieux J, Dupui P, Isableau B, Ohlmann T (1999) Visual contribution to self-induced body sway frequencies and visual perception of male professional dancers. Neurosci Lett 267:189–192

    Google Scholar 

  • Gordon CR, Fletcher WA, Melvill Jones G, Block EW (1995) Adaptive plasticity in the control of locomotor trajectory. Exp Brain Res 102:540–545

    Article  CAS  PubMed  Google Scholar 

  • Gurfinkel VS, Levik YS (1991) Perceptual and automatic aspects of the postural body scheme. In: Paillard J (ed) Brain and space. Oxford University Press, New York, pp 147–162

  • Gurfinkel VS, Lipshits MI, Mori S, Popov KE (1981) Stabilization of body position as the main task of postural regulation. Fiziologiya Cheloveka 7:400–410

    Google Scholar 

  • Gurfinkel VS, Levik YS, Lebedev MA (1989) Immediate and remote postactivation effects in the human motor system. Neirofiziologiya 21:343–351

    CAS  Google Scholar 

  • Gurfinkel VS, Ivanenko YP, Levik YS (1995a) The influence of head rotation on human upright posture during balanced bilateral vibration. NeuroReport 7:137–140

    CAS  PubMed  Google Scholar 

  • Gurfinkel VS, Ivanenko YP, Levik YS, Babakova IA (1995b) Kinesthetic reference for human orthograde posture. Neuroscience 68: 229–243

    Google Scholar 

  • Gurfinkel VS, Levik YS, Kazennikov OV, Selionov VA (1998) Locomotor-like movements evoked by leg muscle vibration in humans. Eur J Neurosci 10:1608–1612

    Google Scholar 

  • Hagbarth KE, Nordin M (1998) Postural after-contractions in man attributed to muscle spindle thixotropy. J Physiol 506.3:875–883

    Google Scholar 

  • Harm DL, Parker DE, Reschke MF, Skinner NC (1998) Relationship between selected orientation rest frame, circular vection and space motion sickness. Brain Res Bull 47:497–501

    Article  CAS  PubMed  Google Scholar 

  • Hlavacka F, Krizkova M, Horak FB (1995) Modification of human postural response to leg muscle vibration by electrical vestibular stimulation. Neurosci Lett 189:9–12

    Google Scholar 

  • Hlavacka F, Mergner T, Krizkova M (1996) Control of the body vertical by vestibular and proprioceptive inputs. Brain Res Bull 40:431–435

    Article  CAS  PubMed  Google Scholar 

  • Horak FB, Hlavacka F (2001) Somatosensory loss increases vestibulospinal sensitivity. J Neurophysiol 86:575–585

    CAS  PubMed  Google Scholar 

  • Isableau B, Ohlmann T, Cremieux J, Amblard B (1997) Selection of spatial frame of reference and postural control variability. Exp Brain Res 114:584–589

    CAS  PubMed  Google Scholar 

  • Isableau B, Ohlmann T, Cremieux J, Amblard B (2003) Differential approach to strategies of segmental stabilisation in postural control. Exp Brain Res 150:208–221

    PubMed  Google Scholar 

  • Ivanenko YP, Talis VL, Kazennikov OV (1999) Support stability influences postural responses to muscle vibration in humans. Eur J Neurosci 11:647–654

    Google Scholar 

  • Ivanenko YP, Grasso M, Lacquaniti F (2000) Neck muscle vibration makes walking humans accelerate in the direction of gaze. J Physiol 525:803–814

    Article  CAS  PubMed  Google Scholar 

  • Kavounoudias A, Roll R, Roll J-P (1998) The plantar sole is a ‘dynamometric map’ for human balance control. NeuroReport 9:3247–3252

    CAS  PubMed  Google Scholar 

  • Kavounoudias A, Gilhodes JC, Roll R, Roll JP (1999) From balance regulation to body orientation: two goals for muscle proprioception information processing? Exp Brain Res 124:80–88

    Article  CAS  PubMed  Google Scholar 

  • Kluzik J, Peterka RJ, Lenzi D, Shupert C, Horak FB (1999) After-effects of prolonged stance on a tilted surface upon postural orientation: vestibular-somatosensory interaction. Gait Posture 9: S34

    Google Scholar 

  • Kluzik J, Peterka RJ, Horak FB (2000) Adaptive plasticity in control of postural orientation revealed by stance and stepping on an incline. Soc Neurosci Abstr 26:169

    Google Scholar 

  • Lackner JR, DiZio P (1994) Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol 72:299–313

    CAS  PubMed  Google Scholar 

  • Lackner JR, DiZio P (2000) Human orientation and movement control in weightless and artificial gravity environments. Exp Brain Res 130:2–26

    Article  CAS  PubMed  Google Scholar 

  • 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 115:300–310

    CAS  PubMed  Google Scholar 

  • Lacquaniti F, Maioli C (1994) Independent control of limb position and contact forces in cat posture. J Neurophysiol 72:1476–1495

    CAS  PubMed  Google Scholar 

  • Lee DN, Lishman JR (1975) Visual proprioceptive control of stance. J Hum Mov Studies 1:87–95

    Google Scholar 

  • Lestienne F, Soechting J, Berthoz A (1977) Postural readjustments induced by linear motion of visual scenes. Exp Brain Res 28:363–384

    CAS  PubMed  Google Scholar 

  • Lund S, Broberg C (1983) Effects of different head positions on postural sway in man induced by a reproducible vestibular error signal. Acta Physiol Scand 117:307–309

    CAS  PubMed  Google Scholar 

  • Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms: II. Specificity and storage of multiple gaze-throw calibrations. Brain 119:1199–1211

    PubMed  Google Scholar 

  • Massion J, Amblard B, Assaiante C, Mouchnino L, Vernazza S (1998) Body orientation and control of coordinated movements in microgravity. Brain Res Rev 28:83–91

    Article  CAS  PubMed  Google Scholar 

  • Maurer C, Mergner T, Bohla B, Hlavacka F (2000) Vestibular, visual, and somatosensory contributions to human control of upright stance. Neurosci Lett 281:99–102

    Article  CAS  PubMed  Google Scholar 

  • Maurer C, Mergner T, Bohla B, Hlavacka F (2001) Human balance control during cutaneous stimulation of the plantar soles. Neurosci Lett 302:45–48

    Article  CAS  PubMed  Google Scholar 

  • McIlroy WE, Maki BE (1997) Preferred placement of the feet during quiet stance: development of a standardized foot placement for balance testing. Clin Biomech 12:66–70

    Google Scholar 

  • Mergner T, Rosemeier T (1998) Interaction of vestibular, somatosensory and visual signals for postural control and motion perception under terrestrial and microgravity conditions—a conceptual model. Brain Res Reviews 28:118–135

    Article  CAS  Google Scholar 

  • Mergner T, Maurer C, Peterka RJ (2002) Sensory contributions to the control of stance. A posture control model. Adv Exp Med Biol 508:147–152

    PubMed  Google Scholar 

  • Mergner T, Maurer C, Peterka RJ (2003) A multisensory posture control model of human upright stance. Prog Brain Res 142:189–201

    Article  CAS  PubMed  Google Scholar 

  • Mittelstaedt H (1996) Somatic graviception. Biol Psychol 42:53–74

    Google Scholar 

  • Mittelstaedt H (1998) Origin and processing of postural information. Neurosci Biobehav Rev 22:473–478

    Google Scholar 

  • Mouchnino L, Aurenty R, Massion J, Pedotti A (1992) Coordination between equilibrium and head-trunk orientation during leg movement: a new strategy built up by training. J Neurophysiol 67:1587–1598

    CAS  PubMed  Google Scholar 

  • Mueller MJ (1996) Identifying patients with diabetes mellitus who are at risk for lower extremity complications: use of Semmes-Weinstein monofilaments. Phys Ther 76:68–71

    CAS  PubMed  Google Scholar 

  • Nashner LM, Wolfson P (1974) Influence of head position and proprioceptive cues on short latency postural reflexes evoked by galvanic stimulation of the human labyrinth. Brain Res 67:255–268

    Article  CAS  PubMed  Google Scholar 

  • Pai Y-C, Patton J (1997) Center of mass velocity-position predictions for balance control J Biomech 30:347–354

    Google Scholar 

  • Perrin P, Deviterne D, Hugel F, Perrot C (2002) Judo, better than dance, develops sensorimotor adaptabilities involved in balance control. Gait Posture 15:187–194

    Article  PubMed  Google Scholar 

  • Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118

    Google Scholar 

  • Quoniam C, Roll JP, Deat A, Massion J (1990) Proprioceptive induced interactions between segmental and whole body posture. In: Brandt T, Paulus W, Bles W, Dieterich M, Krafczyk S, Straube A (eds) Disorders of posture and gait. Georg Thieme Verlag Stuttgart, New York, pp 194–197

  • Rieser JJ, Pick HL, Ashmead DH, Garing AE (1995) Calibration of human locomotion and models of perceptual-motor organization. J Exp Psych Human Percept Perform 21:480–497

    Article  CAS  Google Scholar 

  • Roll J-P, Vedel J-P, Roll R (1989) Eye, head, and skeletal muscle spindle feedback in the elaboration of body references. Prog Brain Res 80:113–123

    CAS  PubMed  Google Scholar 

  • Shumway-Cook A, Horak FB, Yardley L, Bronstein AM (1996) Rehabilitation of balance disorders in the patient with vestibular pathology. In: Bronstein AM, Brandt T, Woollacott MH (eds) Clinical disorders of balance posture and gait. Arnold, London, pp 211–235

  • Slobounov SM, Slobounova ES, Newell KM (1997) Virtual time-to-collision and human postural control. J Mot Behavior 29:263–281

    Google Scholar 

  • Stoffregen TA, Riccio GE (1988) An ecological theory of orientation and the vestibular system. Psychol Rev 95:3–14

    Article  CAS  PubMed  Google Scholar 

  • Vibert N, MacDougall HG, de Waele C, Gilchrist DPD, Burgess AM, Sidis A, Migliaccio A, Curthoys IS, Vidal PP (2001) Variability in the control of head movements in seated humans: a link with whiplash injuries? J Physiol 532.3:851–868

    Google Scholar 

  • Walsh EG (1973) Standing man, slow rhythmic tilting, importance of vision. Aggressologie 14C: 79–85

    Google Scholar 

  • Weber KD, Fletcher WA, Gordon CR, Melvill Jones G, Block EW (1998) Motor learning in the ‘podokinetic system’ and its role in spatial orientation during locomotion. Exp Brain Res 120:377–385

    Article  CAS  PubMed  Google Scholar 

  • Wierzbicka MM, Gilhodes JC, Roll JP (1998) Vibration-induced postural posteffects. J Neurophysiol 79:143–150

    CAS  PubMed  Google Scholar 

  • Witkin HA (1949) Perception of body position and of the position of the visual field. Psychol Monographs 63:1–46

    Google Scholar 

  • Witkin HA, Asch SE (1948) Studies in space orientation. IV. Further experiments on perception of the upright with displaced visual fields. J Exp Psychol 38:762–782

    Google Scholar 

  • Young LR (1984) Perception of the body in space: mechanisms. In: Brookhart JM, Mountcastle VB (eds) Handbook of physiology. Section I. The nervous system, vol III. Sensory processes, part 2, pp 1023–1066

  • Zasorin NL, Baloh RW, Honrubia V (1983) Influence of vestibulo-ocular reflex gain on human optokinetic responses. Exp Brain Res 51:271–274

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by NIH Grant DC04082 to F. Horak, NASA Grant NAG5-7869 and NIH Grant AG17960 to R. Peterka, and an APTA Foundation for Physical Therapy Scholarship to J. Kluzik. The authors thank S. Clark-Donovan and S. Stapley for assistance with data collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fay B. Horak.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kluzik, J., Horak, F.B. & Peterka, R.J. Differences in preferred reference frames for postural orientation shown by after-effects of stance on an inclined surface. Exp Brain Res 162, 474–489 (2005). https://doi.org/10.1007/s00221-004-2124-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-004-2124-6

Keywords

Navigation