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Redirection of gaze and switching of attention during rapid stepping reactions evoked by unpredictable postural perturbation

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Abstract

In many situations successful execution of a balance-recovery reaction requires visual information about the environment. In particular, reactions that involve rapid limb movements, such as stepping, must be controlled to avoid obstacles and accommodate other constraints on limb trajectory. However, it is unknown whether the central nervous system can acquire the necessary visuospatial information prior to perturbation onset or must, instead, redirect gaze at the floor during the execution of the stepping reaction. To study this we examined gaze behaviour, during rapid forward-directed stepping reactions triggered by unpredictable platform perturbation, in 12 healthy young adults. We also monitored switching of attention, as inferred from onset of significant error in performing a concurrent visuomotor tracking task. Obstacles and/or step targets were used as constraints, to increase demands for accurate foot movement. Downward gaze shifts towards the floor almost never occurred during stepping reactions when foot motion was unconstrained but did occur more frequently as the demands for accurate foot movement increased. Nonetheless, even in the most challenging condition (target plus obstacle), downward redirection of gaze occurred in less than 40% of the trials, and subjects were commonly well able to clear the obstacle and land the foot on the target without redirecting their gaze towards the floor. An apparent switching of attention, subsequent to perturbation onset, occurred frequently (>80% of trials) in all task conditions, independent of the gaze shifts. The findings indicate that visual fixation of the foot or floor was not essential for accurate control of the foot movement, nor was the apparent switching of attention that followed perturbation onset linked, in any consistent way, to overt changes in visual fixation. Spatial features of the support surface were apparently “remembered” prior to perturbation onset, thereby allowing both vision and attention to be directed to other demands during the execution of the balance reaction.

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References

  • Abrams RA (1992) Coordination of eye and hand for aimed limb movements. In: Proteau L, Elliot D (eds) Vision and motor control. Elsevier, Amsterdam, pp 129–152

    Google Scholar 

  • Brandt TH, Dichgans J, Koenig E (1973) Differential effects of central versus peripheral vision on egocentric and exocentric motion perception. Exp Brain Res 16:476–491

    Article  CAS  PubMed  Google Scholar 

  • Brauer SG, Woollacott M, Shumway-Cook A (2002) The influence of a concurrent cognitive task on the compensatory stepping response to a perturbation in balance-impaired and healthy elders. Gait Posture 15:83–93

    Article  CAS  PubMed  Google Scholar 

  • Chou LS, Draganich LF, Song SM (1997) Minimum energy trajectories of the swing ankle when stepping over obstacles of different heights. J Biomech 30:115–120

    Article  CAS  PubMed  Google Scholar 

  • Colby CL (1998) Action-oriented spatial reference frames in cortex. Neuron 20:15–24

    Article  CAS  PubMed  Google Scholar 

  • Di Fabio RP, Zampieri C, Greany JF (2003) Aging and saccade-stepping interactions in humans. Neurosci Lett 339:179–182

    Article  CAS  PubMed  Google Scholar 

  • Diener HC, Dichgans J, Guschlbauer B, Bacher M (1986) Role of visual and static vestibular influences on dynamic postural control. Hum Neurobiol 5:105–113

    CAS  PubMed  Google Scholar 

  • Ghafouri M, McIlroy WE, Maki BE (2004) Initiation of rapid reach-and-grasp balance reactions: is a pre-formed visuospatial map used in controlling the initial arm trajectory? Exp Brain Res 155:532–536

    Article  PubMed  Google Scholar 

  • Harris LR, Jenkin M (2001) Vision and attention. In: Jenkin M, Harris LR (eds) Vision and attention. Springer, Berlin Heidelberg New York, pp 2–17

    Google Scholar 

  • Hollands MA, Marple-Horvat DE (1996) Visually guided stepping under conditions of step cycle-related denial of visual information. Exp Brain Res 109:343–356

    Article  CAS  PubMed  Google Scholar 

  • Hollands MA, Marple-Horvat DE (2001) Coordination of eye and leg movements during visually guided stepping. J Mot Behav 33:205–216

    CAS  PubMed  Google Scholar 

  • Hollands MA, Marple-Horvat DE, Henkes S, Rowan AK (1995) Human eye movements during visually guided stepping. J Mot Behav 27:155–163

    PubMed  Google Scholar 

  • Hsiao ET, Robinovitch SN (1999) Biomechanical influences on balance recovery by stepping. J Biomech 32:1099–1106

    Article  CAS  PubMed  Google Scholar 

  • Hunter MC, Hoffman MA (2001) Postural control: visual and cognitive manipulations. Gait Posture 13:41–48

    Article  CAS  PubMed  Google Scholar 

  • Lyon D (1990) Large and rapid improvement in form discrimination accuracy following a location precue. Acta Psychol 73:69–82

    Article  CAS  Google Scholar 

  • Maki BE, McIlroy WE (1997) The role of limb movements in maintaining upright stance: the “change-in-support” strategy. Phys Ther 77:488–507

    CAS  PubMed  Google Scholar 

  • Maki BE, McIlroy WE (1999) The control of foot placement during compensatory stepping reactions: does speed of response take precedence over stability?. IEEE Trans Rehabil Eng 7:80–90

    Article  CAS  PubMed  Google Scholar 

  • Maki BE, Norrie RG, Zecevic A, Quant S, Kirshenbaum N, Bateni H, McIlroy WE (2001a) Initiation and execution of rapid postural reactions and stepping movements: which phases require visuospatial attention? In: Duysens J, Smits-Engelsman BCM, Kingma H (eds) Control of posture and gait. International Society for Postural and Gait Research, Maastricht, The Netherlands, pp 573–576

    Google Scholar 

  • Maki BE, Zecevic A, Bateni H, Kirshenbaum N, McIlroy WE (2001b) Cognitive demands of executing rapid postural reactions: does aging impede attentional switching? NeuroReport 12:3583–3587

    Article  CAS  PubMed  Google Scholar 

  • Maki BE, McIlroy WE, Fernie GR (2003) Change-in-support reactions for balance recovery: control mechanisms, age-related changes and implications for fall prevention. IEEE Eng Med Biol Mag 22:20–26

    Article  Google Scholar 

  • McFadden S, Wallman J (2001) Shifts of attention and saccades are very similar: are they causally linked?. In: Jenkin M, Harris LR (eds) Vision and attention. Springer, Berlin Heidelberg New York, pp 19–39

    Google Scholar 

  • McIlroy WE, Maki BE (1995) Early activation of arm muscles follows external perturbations of upright stance. Neurosci Lett 184:177–180

    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

    Article  Google Scholar 

  • McIlroy WE, Norrie RG, Brooke JD, Bishop DC, Nelson AJ, Maki BE (1999) Temporal properties of attention sharing consequent to disturbed balance. NeuroReport 10:2895–2899

    CAS  PubMed  Google Scholar 

  • Norrie RG, Maki BE, Staines WR, McIlroy WE (2002) The time course of attention shifts following perturbation of upright stance. Exp Brain Res 146:315–321

    Article  PubMed  Google Scholar 

  • Pai YC (2003) Movement termination and stability in standing. Exerc Sports Sci Rev 31:19–25

    Article  Google Scholar 

  • Patla AE, Vickers JN (1997) Where and when do we look as we approach and step over an obstacle in the travel path? NeuroReport 8:3661–3665

    CAS  PubMed  Google Scholar 

  • Quant S, Adkin A, Staines WR, Maki BE, McIlroy WE (2004) The effect of a concurrent cognitive task on cortical potentials evoked by unpredictable balance perturbations. Biomed Cent Neurosci 5:18

    Article  Google Scholar 

  • Rankin J, Woollacott MH, Shumway-Cook A, Brown L (2000) Cognitive influence on postural stability: a neuromuscular analysis in young and elders. J Gerontol 55A:M112–M119

    CAS  Google Scholar 

  • Redfern MS, Jennings JR, Martin C, Furman JM (2001) Attention influences sensory integration for postural control in older adults. Gait Posture 14:211–216

    Article  CAS  PubMed  Google Scholar 

  • Redfern MS, Muller ML, Jennings JR, Furman JM (2002) Attentional dynamics in postural control during perturbations in young and older adults. J Gerontol 57:B298–B303

    Google Scholar 

  • Shumway-Cook A, Woollacott M (2000) Attentional demands and postural control: the effect of sensory context. J Gerontol 55A:M10–M16

    CAS  Google Scholar 

  • Zettel JL, McIlroy WE, Maki BE (2002a) Can stabilizing features of rapid triggered stepping reactions be modulated to meet environmental constraints? Exp Brain Res 145:297–308

    Article  PubMed  Google Scholar 

  • Zettel JL, McIlroy WE, Maki BE (2002b) Environmental constraints on foot trajectory reveal the capacity for modulation of anticipatory postural adjustments during rapid triggered stepping reactions. Exp Brain Res 146:38–47

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by grants from the Canadian Institutes of Health Research (CIHR) and the Ontario Neurotrauma Foundation. B.E.M. was a CIHR Senior Investigator and W.E.M. held a Canada Research Chair in neuro-rehabilitation. J.L.Z. held scholarships from the Natural Sciences and Engineering Research Council and from the Health Care, Technology and Place Program (University of Toronto).

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Authors and Affiliations

  1. Centre for Studies in Aging , Sunnybrook and Women’s College Health Sciences Centre, University of Toronto, 2075 Bayview Avenue, Toronto, Ontario, M4N 3M5, Canada

    John L. Zettel, Andrea Holbeche, William E. McIlroy & Brian E. Maki

  2. Institute of Medical Science, University of Toronto, Canada

    Brian E. Maki

  3. Institute of Biomaterials and Biomedical Engineering, University of Toronto, Canada

    Brian E. Maki

  4. Graduate Department of Rehabilitation Science, University of Toronto, Canada

    William E. McIlroy

Authors
  1. John L. Zettel
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  2. Andrea Holbeche
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  3. William E. McIlroy
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  4. Brian E. Maki
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Corresponding author

Correspondence to Brian E. Maki.

Additional information

Presented (in part) at the 16th International Symposium on Posture and Gait (Sydney, Australia; March 2003), the 13th Biennial Conference of the Canadian Society for Biomechanics (Halifax, Canada; August 2004), and the 34th Annual Meeting of the Society for Neuroscience (San Diego, California; October 2004).

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Zettel, J.L., Holbeche, A., McIlroy, W.E. et al. Redirection of gaze and switching of attention during rapid stepping reactions evoked by unpredictable postural perturbation. Exp Brain Res 165, 392–401 (2005). https://doi.org/10.1007/s00221-005-2310-1

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  • DOI: https://doi.org/10.1007/s00221-005-2310-1

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