Abstract
Several studies in adults having observed the effect of eye movements on postural control provided contradictory results. In the present study, we explored the effect of various oculomotor tasks on postural control and the effect of different postural tasks on eye movements in eleven children (7.8 ± 0.5 years) and nine adults (30.4 ± 6.3 years). To vary the difficulty of the oculomotor task, three conditions were tested: fixation, prosaccades (reactive saccades made toward the target) and antisaccades (voluntary saccades made in the direction opposite to the visual target). To vary the difficulty of postural control, two postural tasks were tested: Standard Romberg (SR) and Tandem Romberg (TR). Postural difficulty did not affect oculomotor behavior, except by lengthening adults’ latencies in the prosaccade task. For both groups, postural control was altered in the antisaccade task as compared to fixation and prosaccade tasks. Moreover, a ceiling effect was found in the more complex postural task. This study highlighted a cortical interference between oculomotor and postural control systems.
Similar content being viewed by others
Notes
We run statisical analyses on postural variables in the antero-posterior direction. Very similar results to that of ML direction presented further in the text were found.
References
Abernethy B (1988) Dual-task methodology and motor skills research: some methodological constraints. J Hum Mov Stud 14:101–132
Ajrezo L, Wiener-Vacher S, Bucci MP (2013) Saccades improve postural control: a developmental study in normal children. PLoS One 8(11):e81066. doi:10.1371/journal.pone.0081066
Andersson G, Hagman J, Talianzadeh R, Svedberg A, Larsen HC (2002) Effect of cognitive load on postural control. Brain Res Bull 58:135–139
Aring E, Grönlund MA, Hellström A, Ygge J (2007) Visual fixation development in children. Graefes Arch Clin Exp Opthalmol 245:1659–1665
Assaiante C, Amblard B (1995) An ontogenetic model for the sensorimotor organization of balance control in humans. Hum Mov Sci 14:13–43
Assaiante C, Mallau S, Viel S, Jover M, Schmitz C (2005) Development of postural control in healthy children: a functional approach. Neural Plast 12(2–3):109–118
Barra J, Bray A, Sahni V, Golding JF, Gresty MA (2006) Increasing cognitive load with increasing balance challenge: recipe for catastrophe. Exp Brain Res 174(4):734–745
Becker W (1989) The neurobiology of saccadic eye movements. Metrics Rev Oculomot Res 3:13–67
Blanchard Y, Carey S, Coffey J, Cohen A, Harris T, Michlik S, Pellecchia GL (2005) The influence of concurrent cognitive tasks on postural sway in children. Pediatr Phys Ther Fall 17(3):189–193
Bucci MP, Seassau M (2012) Saccadic eye movements in children: a developmental study. Exp Brain Res 222(1–2):21–30
Courchesne E, Chisum HJ, Townsend J, Cowles A, Covington J, Egaas B, Harwood M, Hinds S, Press GA (2000) Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Neuroradiol 216:672–682
Day BL, Steiger MJ, Thompson PD, Marsden CD (1993) Effect of vision and stance width on human body motion when standing: implications for afferent control of lateral sway. J Physiol 469:479–499
Di Russo FD, Pitzalis S, Spinelli D (2003) Fixation stability and saccadic latency in elite shooters. Vis Res 43:1837–1845
Ettinger U, Ffytche DH, Kumari V, Kathmann N, Reuter B, Zelaya F et al (2008) Decomposing the neural correlates of anti-saccade eye movements using event-related FMRI. Cereb Cortex 18(5):1148–1159
Everling S, Fischer B (1998) The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36:885–899
Everling S, Munoz DP (2000) Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20(1):387–400
Fischer B, Weber H (1997) Effects of stimulus conditions on the performance of antisaccades in man. Exp Brain Res 116:191–200
Fraizer EV, Mitra S (2008) Methodological and interpretive issues in posture-cognition dual tasking in upright stance. Gait Posture 27:271–279
Fukushima J, Hatta T, Fukushima K (2000) Development of voluntary control of saccadic eye movements. I. Age-related changes in normal children. Brain Dev 22:173–180
Geurts AC, Nienhuis B, Mulder TW (1993) Intrasubject variability of selected force-platform parameters in the quantification of postural control. Arch Phys Med Rehabil 74:1144–1150
Glasauer S, Schneider E, Jahn K, Strupp M, Brandt T (2005) How the eyes move the body. Neurology 65(8):1291–1293
Glickstein M (2000) How are visual areas of the brain connected to motor areas for the sensory guidance of movement? Trends Neurosc 23:613–617
Goldberg ME, Bushnell MC, Bruce CJ (1986) The effect of attentive fixation on eye movements evoked by electrical stimulation of the frontal eye fields. Exp Brain Res 61:579–584
Guerraz M, Bronstein AM (2008) Ocular versus extraocular control of posture and equilibrium. Clin Neurophysiol 38:391–398
Hallett P (1978) Primary and secondary saccades to goals defined by instructions. Vis Res 18:1279–1296
Hallett P (1986) Eye movements. In: Boff KR, Kaufman L, Thomas JP (eds) Handbook of human perception and performance, vol 1. Wiley, New York
Horak AFB, Nashner LM, Diener HC (1990) Postural strategies associated with somatosensory and vestibular loss. Exp Brain Res 82:167–177
Hunter MC, Hoffman MA. (2001) Postural control: visual and cognitive manipulations. Gait Posture 13(1):41–48
Hutton SB (2008) Cognitive control of saccadic eye movements. Brain Cog 68:327–340
Huxhold O, Li SC, Schmiedek F, Lindenberger U (2006) Dual tasking postural control: aging and the effects of cognitive demand in conjunction with focus of attention. Brain Res Bul 69:294–305
Jacobs JV, Horak FB (2007) Cortical control of postural responses. J Neural Transm 114:1339–1348
Kerr B, Condon SM, McDonald LA (1985) Cognitive spatial processing and the regulation of posture. J Exp Psychol 11:617–622
Klein C (2001) Developmental functions for saccadic eye movement parameters derived from pro- and antisaccade tasks. Exp Brain Res 139:1–17
Lajoie Y, Teasdale N, Bard C, Fleury M (1993) Attentional demands for static and dynamic equilibrium. Exp Brain Res 97(1):139–144
Leigh RJ, Zee DS (2006) The neurology of eye movement, 4th edn. Oxford University Press, New York
Legrand A, Doré-Mazars K, Lazzareschi J, Lemoine C, Olivier I, Barra J, Bucci MP (2013) Prosaccades and antisaccades affect in a different way postural stability. Exp Brain Res 227(3):397–405
Luna B, Thulborn KR, Munoz DP, Merriam EP, Garver KE, Minshew NJ et al (2001) Maturation of widely distributed brain function subserves cognitive development. Neuroimage 13:786–793
Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA (2004) Maturation of cognitive processes from late childhood to adulthood. Child Dev 75:1357–1372
Luna B, Velanova K, Geier CF (2008) Development of eye movement control. Brain Cognit 68(3):293–308
Maki B, Holliday P, Fernie G (1990) Aging and postural control: a comparison of spontaneous- and induced-way balance tests. J Am Geriatr Soc 38:1–9
Matsuda T, Matsuura M, Ohkubo T, Ohkubo H, Matsushima E, Inoue K et al (2004) Functional MRI mapping of brain activation during visually guided saccades and anti-saccades: Cortical and subcortical networks. Psychiatry Res 131(2):147–155
Mountcastle VB, Andersen RA, Motter BC (1981) The influence of attentive fixation upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J Neurosci 1:1218–1225
Munoz DP, Broughton JR, Goldring JE, Armstrong IT (1998) Age-related performance of human subjects on saccadic eye movement tasks. Exp Brain Res 121:391–400
Munoz DP, Wurtz RH (1992) Role of the rostral superior colliculus in active visual fixation and execution of express saccades. J Neurophysiol 67:1000–1002
Nashner LM (1976) Adapting reflexes controlling the human posture. Exp Brain Res 26:59–72
Nieuwenhuis S, Broerse A, Nielen MMA, de Jong R (2004) A goal activation approach to the study of executive function: an application to antisaccade tasks. Brain Cogn 56:198–214
Olivier I, Palluel E, Nougier V (2008) Effects of attentional focus on postural sway in children and adults. Exp Brain Res 185:341–345
Olivier I, Cuisinier R, Vaugoyeau M, Nougier V, Assaiante C (2010) Age-related differences in cognitive and postural dual-task performance. Gait Posture 32(4):494–499
Otero-Millan J, Troncoso XG, Macknik SL, Serrano Pedraza I, Martinez-Conde S (2008) Saccades and microsaccades during visual fixation, exploration, and search: foundations for a common saccadic generator. J Vis 8(14):21.1–21.18
Ouchi Y, Okada H, Yoshikawa E, Nobezawa S, Futatsubashi M (1999) Brain activation during maintenance of standing postures in humans. Brain 122:329–338
Pierrot-Deseilligny CH, Rivaud S, Gaymard B, Agid Y (1991) Cortical control of reflexive visually guided saccades. Brain 114:1473–1485
Pellecchia GL (2003) Postural sway increases with attentional demands of concurrent cognitive task. Gait Posture 18:29–34
Rizzolatti G, Riggio L, Dascol I, Umiltà C (1987) Reorienting attention across the vertical and horizontal meridians: evidence in favor of a premotor theory of attention. Neuropsychologia 25:31–40
Rodrigues ST, Polastri PF, Carvalho JC, Barela JA, Moraes R, Barbieri FA (2015) Saccadic and smooth pursuit eye movements attenuate postural sway similarly. Neurosci Lett 1(584):292–295
Ross S, Ross L (1980) Saccade latency and warning signals: stimulus onset, offset, and change as warning events. Percept Psychophys 27:251–257
Rougier P, Garin M (2007) Performing saccadic eye movements or blinking improves postural control. Mot Control 11(3):213–223
Schaefer S, Krampe RT, Lindenberger U, Baltes PB (2008) Age differences between children and young adults in the dynamics of dual-task prioritization: body (balance) versus mind (memory). Dev Psychol 44:747–757
Schärli AM, van de Langenberg R, Murer K, Müller RM (2012) The influence of gaze behavior on postural control from early childhood into adulthood. Gait Posture 36(1):78–84
Shumway-Cook A, Woollacott MH (1985) The growth of stability: postural control from a developmental perspective. J Mot Behav 17:131–147
Smyrnis N, Kattoulas E, Evdokimidis I, Stefanis NC, Avramopoulos D, Pantes G, Theleritis C, Stefanis SN (2004) Active eye fixation performance in 940 young men: Effects of IQ, schizotypy, anxiety and depression. Exp Brain Res 156:1–10
Stoffregen TA, Hove P, Schmit J, Bardy BG (2006) Voluntary and involuntary postural responses to imposed optic flow. Mot Control 10(1):24–33
Stoffregen TA, Bardy BG, Bonnet CT, Hove P, Oullier O (2007) Postural sway and the frequency of horizontal eye movements. Mot Control 11(1):86–102
Straube A, Paulus W, Quintern J, Brandt T (1989) Visual ataxia induced by eye movements: posturographic measurements in normal and patients with ocular motor disorders. Clin Vis Sci 4(2):107–113
Uchida T, Hashimoto M, Suzuki N, Takegami T, Iwase I (1979) Effects of periodic saccades on the body sway in human subjects. Neurosci Lett 13:253–258
White KD, Post RB, Leibowitz HW (1980) Saccadic eye movements and body sway. Science 208(4444):621–623
Wydenkeller S, Liechti M, Müller R, Curt A (2006) Impaired scaling of responses to vestibular stimulation in incomplete SCI. Exp Brain Res 175:191–195
Ygge J, Aring E, Han Y, Bolzani R, Hellström A (2005) Fixation stability in normal children. An New York AcadSci 1039:480–483
Acknowledgments
Authors are grateful to the children and to their parents for their precious collaboration.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest statement
Authors had no financial and personal relationships with other people or organizations that could inappropriately influence or bias their work in this study.
Rights and permissions
About this article
Cite this article
Legrand, A., Doré Mazars, K., Lemoine, C. et al. Interference between oculomotor and postural tasks in 7–8-year-old children and adults. Exp Brain Res 234, 1667–1677 (2016). https://doi.org/10.1007/s00221-016-4565-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-016-4565-0