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Experimental Brain Research

, Volume 226, Issue 4, pp 549–556 | Cite as

Constraining eye movement when redirecting walking trajectories alters turning control in healthy young adults

  • V. N. Pradeep Ambati
  • Nicholas G. Murray
  • Fabricio Saucedo
  • Douglas W. Powell
  • Rebecca J. Reed-JonesEmail author
Research Article

Abstract

Humans use a specific steering synergy, where the eyes and head lead rotation to the new direction, when executing a turn or change in direction. Increasing evidence suggests that eye movement is critical for turning control and that when the eyes are constrained, or participants have difficulties making eye movements, steering control is disrupted. The purpose of the current study was to extend previous research regarding eye movements and steering control to a functional walking and turning task. This study investigated eye, head, trunk, and pelvis kinematics of healthy young adults during a 90° redirection of walking trajectory under two visual conditions: Free Gaze (the eyes were allowed to move naturally in the environment), and Fixed Gaze (participants were required to fixate the eyes on a target in front). Results revealed significant differences in eye, head, and trunk coordination between Free Gaze and Fixed Gaze conditions (p < 0.001). During Free Gaze, the eyes led reorientation followed by the head and trunk. Intersegment timings between the eyes, head, and trunk were significantly different (p < 0.05). In contrast, during Fixed Gaze, the segments moved together with no significant differences between segment onset times. In addition, the sequence of segment rotation during Fixed Gaze suggested a bottom-up postural perturbation control strategy in place of top-down steering control seen in Free Gaze. The results of this study support the hypothesis that eye movement is critical for the release of the steering synergy for turning control.

Keywords

Locomotion Steering control Turning Eye movements Oculomotor Basal ganglia 

Notes

Acknowledgments

This work was supported by the University Research Institute (URI) program at The University of Texas at El Paso (UTEP). VNPA and NGM were supported by graduate research awards from the College of Health Sciences (UTEP).

References

  1. Assaiante C (1998) Development of locomotor balance control in healthy children. Neurosci Biobehav Rev 22(4):527–532PubMedCrossRefGoogle Scholar
  2. Bernstein N (1967) The coordination and regulation of movements. Pergamon Press, Oxford, London, p 196Google Scholar
  3. Crenna P, Carpinella I, Rabuffetti M, Calabrese E, Mazzoleni P, Nemni R, Ferrarin M (2007) The association between impaired turning and normal straight walking in Parkinson’s disease. Gait Posture 26:172–178PubMedCrossRefGoogle Scholar
  4. Earhart GM, Hong M (2006) Kinematics of podokinetic after-rotation: similarities to voluntary turning and potential clinical implications. Brain Res Bull 70(1):15–21PubMedCrossRefGoogle Scholar
  5. Fawcett AP, Dostrovsky JO, Lozano AM, Hutchison WD (2005) Eye movement-related responses of neurons in human subthalamic nucleus. Exp Brain Res 162:357–365PubMedCrossRefGoogle Scholar
  6. Folstein MF, Folstein SE, McHugh PR (1975) “Mini mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatry Res 12(1):89–98Google Scholar
  7. Glaister BC, Bernatz GC, Klute GK, Orendurff MS (2007) Video task analysis of turning during activities of daily living. Gait Posture 25:289–294PubMedCrossRefGoogle Scholar
  8. Grasso R, Prevost P, Ivanenko YP, Berthoz A (1998) Eye-head coordination for the steering of locomotion in humans: an anticipatory synergy. Neurosci Lett 253:115–118PubMedCrossRefGoogle Scholar
  9. Hicheur H, Vieilledent S, Berthoz A (2005) Head motion in humans alternating between straight and curved walking path: combination of stabilizing and anticipatory orienting mechanisms. Neurosci Lett 383:87–92PubMedCrossRefGoogle Scholar
  10. Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953–978PubMedGoogle Scholar
  11. Hollands MA, Sorensen KL, Patla AE (2001) Effects of head immobilization on the coordination and control of head and body reorientation and translation during steering. Exp Brain Res 140:223–233PubMedCrossRefGoogle Scholar
  12. Hollands MA, Patla AE, Vickers JN (2002) “Look where you’re going!”: gaze behavior associated with maintaining and changing the direction of locomotion. Exp Brain Res 143:221–230PubMedCrossRefGoogle Scholar
  13. Hollands MA, Ziavra NV, Bronstein AM (2004) A new paradigm to investigate the roles of head and eye movements in the coordination of whole-body movements. Exp Brain Res 154:261–266PubMedCrossRefGoogle Scholar
  14. Hollands KL, van Vliet P, Zietz D, Wing A, Wright C, Hollands MA (2010) Stroke-related differences in axial body segment coordination during preplanned and reactive changes in walking direction. Exp Brain Res 202:591–604PubMedCrossRefGoogle Scholar
  15. Horak F, Nashner L (1986) Central programming of postural control movements: adaptation to altered support-surface configurations. J Neurophysiol 55(6):1369–1381PubMedGoogle Scholar
  16. Hyndman D, Ashburn A, Stack E (2002) Fall events among people with stroke living in the community: circumstances of falls and characteristics of fallers. Arch Phys Med Rehabil 83:165–170PubMedCrossRefGoogle Scholar
  17. Imai T, Moore ST, Raphan T, Cohen B (2001) Interaction of body, head, and eyes during walking and turning. Exp Brain Res 136:1–18PubMedCrossRefGoogle Scholar
  18. Lamontagne A, De Serres SJ, Fung J, Paquet N (2005) Stroke affects the coordination and stabilization of head, thorax and pelvis during voluntary horizontal head motions performed in walking. Clin Neurophysiol 116:101–111PubMedCrossRefGoogle Scholar
  19. Lamontagne A, Paquette C, Fung J (2007) Stroke affects the coordination of gaze and posture during preplanned turns while walking. Neurorehabil Neural Repair 21:62–67PubMedCrossRefGoogle Scholar
  20. Land MF, Furneaux S (1997) The knowledge base of the oculomotor system. JSTOR: Philos Trans Biol Sci 352:1231–1239CrossRefGoogle Scholar
  21. Lohnes CA, Earhart GM (2011) Saccadic eye movements are related to turning performance in Parkinson’s disease. J Parkinsons Dis 1(1):109–118PubMedGoogle Scholar
  22. Mak MK, Patla A, Hui-Chan C (2008) Sudden turn during walking is impaired in people with Parkinson’s disease. Exp Brain Res 190(1):43–51PubMedCrossRefGoogle Scholar
  23. Matsumara M, Kojima J, Gardiner T, Hikosaka O (1992) Visual and oculomotor functions of monkey subthalamic nucleus. J Neurophysiol 67:1615–1632Google Scholar
  24. Paquette MR, Fuller JR, Adkin AL, Vallis LA (2008) Age-related modifications in steering behaviour: effects of base-of-support constraints at the turn point. Exp Brain Res 190:1–9PubMedCrossRefGoogle Scholar
  25. Patla AE, Prentice SD, Robinson C, Neufeld J (1991) Visual control of locomotion: strategies for changing direction and for going over obstacles. J Exp Psychol 17(3):603–634Google Scholar
  26. Patla AE, Adkin A, Ballard T (1999) Online steering: coordination and control of body center of mass, head and body reorientation. Exp Brain Res 129:629–634PubMedCrossRefGoogle Scholar
  27. Reed-Jones RJ, Vallis LA (2007) Proprioceptive deficits of the lower limb following anterior cruciate ligament deficiency affect whole body steering control. Exp Brain Res 182:249–260PubMedCrossRefGoogle Scholar
  28. Reed-Jones RJ, Hollands MA, Reed-Jones JG, Vallis LA (2009a) Visually evoked whole-body turning responses during stepping in place in a virtual environment. Gait Posture 30:317–321PubMedCrossRefGoogle Scholar
  29. Reed-Jones R, Reed-Jones J, Vallis LA, Hollands MA (2009b) The effects of constraining eye movements on visually evoked steering responses during walking in a virtual environment. Exp Brain Res 197:357–367PubMedCrossRefGoogle Scholar
  30. Ting L, Macpherson J (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609–613PubMedCrossRefGoogle Scholar
  31. Torres-Oviedo G, Ting L (2007) Muscle synergies characterizing human postural responses. J Neurophysiol 98:2144–2156PubMedCrossRefGoogle Scholar
  32. Torres-Oviedo G, Macpherson J, Ting L (2006) Muscle synergy organization is robust across a variety of postural perturbations. J Neurophysiol 96:1530–1546PubMedCrossRefGoogle Scholar
  33. Vallis LA, McFadyen BJ (2003) Locomotor adjustments for circumvention of an obstacle in the travel path. Exp Brain Res 152:409–414PubMedCrossRefGoogle Scholar
  34. Wright RL, Peters DM, Robinson PD, Sitch AJ, Watt TN, Hollands MA (2012) Differences in axial segment reorientation during standing turns predict multiple falls in older adults. Gait Posture 36(3):541–545PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • V. N. Pradeep Ambati
    • 1
  • Nicholas G. Murray
    • 1
  • Fabricio Saucedo
    • 2
  • Douglas W. Powell
    • 3
  • Rebecca J. Reed-Jones
    • 2
    • 4
    Email author
  1. 1.Interdisciplinary Health Sciences PhD ProgramThe University of Texas at El PasoEl PasoUSA
  2. 2.Department of Kinesiology, College of Health SciencesThe University of Texas at El PasoEl PasoUSA
  3. 3.Department of Physical TherapyCampbell UniversityBuies CreekUSA
  4. 4.Physical Therapy Program, Department of Rehabilitation, College of Health SciencesThe University of Texas at El PasoEl PasoUSA

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