Visually-guided saccades attenuate postural sway under non-fatigued, fatigued, and stretched states

Abstract

Muscular fatigue, which reduces force output and position sense, often leads to increased sway and potential balance impairments. In contrast, visually-guided saccadic eye movements (saccades) can attenuate sway more than fixating gaze on an external target. The goals of this study were to determine whether the use of saccades could reduce the increased postural sway in a fatigued state and to better understand the contributions to fatigue-induced increased sway. We compared the effects of gazing at a fixation point (FP) and performing saccades (SAC) on various spatial and temporal measures of the center of pressure (CoP) while participants stood as still as possible on a force plate. Participants used either a narrow or wide base of support and performed three trials for each eye movement condition (SAC, FP) in three states (non-fatigued—NF, stretched—S, and fatigued—F). Calf raises to exhaustion induced ankle fatigue. Extreme plantar- and dorsi-flexion induced stretch. SAC significantly decreased sway and increased time-series complexity (sample entropy) compared to FP. F increased sway and decreased time-series complexity compared to NF and S states, which were similar. Reduced force production, which accompanies muscle fatigue and stretching, did not account for increased sway associated with acute bouts of ankle muscle fatigue. Increased position sense often associated with muscle stretching likely compensated for any reduced force output for S, while the decreased position sense associated with F probably explained the increased sway in this state. Performing saccadic eye movements during quiet stance can help reduce sway under various states.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abd-Elfattah HM, Abdelazeim FH, Elshennawy S (2015) Physical and cognitive consequences of fatigue: a review. J Adv Res 6:351–358. https://doi.org/10.1016/j.jare.2015.01.011

    Article  PubMed  PubMed Central  Google Scholar 

  2. Aguiar SA, Polastri PF, Godoi D, Moraes R, Barela JA, Rodrigues ST (2015) Effects of saccadic eye movements on postural control in older adults. Psychol Neurosci 8:19–27

    Article  Google Scholar 

  3. Ajrezo L, Wiener-Vacher S, Bucci MP (2013) Saccades improve postural control: a developmental study in normal children. PLoS One 8:e81066. https://doi.org/10.1371/journal.pone.0081066

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bisson EJ, Lajoie Y, Bilodeau M (2014) The influence of age and surface compliance on changes in postural control and attention due to ankle neuromuscular fatigue. Exp Brain Res 232:837–845. https://doi.org/10.1007/s00221-013-3795-7

    Article  PubMed  Google Scholar 

  5. Bjorklund M, Djupsjobacka M, Crenshaw AG (2006) Acute muscle stretching and shoulder position sense. J Athl Train 41:270–274

    PubMed  PubMed Central  Google Scholar 

  6. Borg FG, Laxaback G (2010) Entropy of balance—some recent results. J Neuroeng Rehabil 7:38. https://doi.org/10.1186/1743-0003-7-38

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bottoni G, Heinrich D, Kofler P, Hasler M, Nachbauer W (2015) The effect of uphill and downhill walking on joint-position sense: a study on healthy knees. J Sport Rehabil 24:349–352. https://doi.org/10.1123/jsr.2014-0192

    Article  PubMed  Google Scholar 

  8. Chandra S, Hayashibe M, Thondiyath A (2014) Dominant component in muscle fatigue induced hand tremor during laparoscopic surgical manipulation. Conf Proc IEEE Eng Med Biol Soc 2014:6539–6542. https://doi.org/10.1109/EMBC.2014.6945126

    Article  PubMed  Google Scholar 

  9. Cho SH, Kim SH (2016) Immediate effect of stretching and ultrasound on hamstring flexibility and proprioception. J Phys Ther Sci 28:1806–1808. https://doi.org/10.1589/jpts.28.1806

    Article  PubMed  PubMed Central  Google Scholar 

  10. Cornwell A, Nelson AG, Sidaway B (2002) Acute effects of stretching on the neuromechanical properties of the triceps surae muscle complex. Eur J Appl Physiol 86:428–434. https://doi.org/10.1007/s00421-001-0565-1

    Article  PubMed  Google Scholar 

  11. Coubard OA (2012) Fall prevention modulates decisional saccadic behavior in aging. Front Aging Neurosci 4:18. https://doi.org/10.3389/fnagi.2012.00018

    Article  PubMed  PubMed Central  Google Scholar 

  12. Donath L, Kurz E, Roth R, Zahner L, Faude O (2016) Leg and trunk muscle coordination and postural sway during increasingly difficult standing balance tasks in young and older adults. Maturitas 91:60–68. https://doi.org/10.1016/j.maturitas.2016.05.010

    Article  PubMed  Google Scholar 

  13. Fox CR (1990) Some visual influences on human postural equilibrium: binocular versus monocular fixation. Percept Psychophys 47:409–422

    CAS  Article  Google Scholar 

  14. Ghaffarinejad F, Taghizadeh S, Mohammadi F (2007) Effect of static stretching of muscles surrounding the knee on knee joint position sense. Br J Sports Med 41:684–687. https://doi.org/10.1136/bjsm.2006.032425

    Article  PubMed  PubMed Central  Google Scholar 

  15. Haran FJ, Keshner EA (2008) Sensory reweighting as a method of balance training for labyrinthine loss. J Neurol Phys Ther 32:186–191. https://doi.org/10.1097/NPT.0b013e31818dee39

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Hemmati L, Rojhani-Shirazi Z, Ebrahimi S (2016) Effects of plantar flexor muscle static stretching alone and combined with massage on postural balance. Ann Rehabil Med 40:845–850. https://doi.org/10.5535/arm.2016.40.5.845

    Article  PubMed  PubMed Central  Google Scholar 

  17. Hondzinski JM, Li L, Welsch M (2010) Age-related and sensory declines offer insight to whole body control during a goal-directed movement. Mot Control 14:176–194

    Article  Google Scholar 

  18. Kim SY, Moon BY, Cho HG (2016) Smooth-pursuit eye movements without head movement disrupt the static body balance. J Phys Ther Sci 28:1335–1338. https://doi.org/10.1589/jpts.28.1335

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kouzaki M, Masani K (2012) Postural sway during quiet standing is related to physiological tremor and muscle volume in young and elderly adults. Gait Posture 35(1):11–17. https://doi.org/10.1016/j.gaitpost.2011.03.028

    Article  PubMed  Google Scholar 

  20. Lamoth CJC, van Lummel RC, Beek PJ (2009) Athletic skill level is reflected in body sway: a test case for accelometry in combination with stochastic dynamics. Gait Posture 29:546–551. https://doi.org/10.1016/j.gaitpost.2008.12.006

    Article  PubMed  Google Scholar 

  21. Larsen R, Lund H, Christensen R, Rogind H, Danneskiold-Samsoe B, Bliddal H (2005) Effect of static stretching of quadriceps and hamstring muscles on knee joint position sense. Br J Sports Med 39:43–46. https://doi.org/10.1136/bjsm.2003.011056

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Ledin T, Fransson PA, Magnusson M (2004) Effects of postural disturbances with fatigued triceps surae muscles or with 20% additional body weight. Gait Posture 19:184–193. https://doi.org/10.1016/S0966-6362(03)00061-4

    Article  PubMed  Google Scholar 

  23. Lubetzky AV, Harel D, Lubetzky E (2018) On the effects of signal processing on sample entropy for postural control. PLoS One 13:e0193460. https://doi.org/10.1371/journal.pone.0193460

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Mohapatra S, Krishnan V, Aruin AS (2012) Postural control in response to an external perturbation: effect of altered proprioceptive information. Exp Brain Res 217:197–208. https://doi.org/10.1007/s00221-011-2986-3

    Article  PubMed  Google Scholar 

  25. Nagano A, Yoshioka S, Hay DC, Himeno R, Fukashiro S (2006) Influence of vision and static stretch of the calf muscles on postural sway during quiet standing. Hum Mov Sci 25:422–434. https://doi.org/10.1016/j.humov.2005.12.005

    Article  PubMed  Google Scholar 

  26. Nelson AG, Kokkonen J (2014) Stretching anatomy. Human Kinetics, Champaign

    Google Scholar 

  27. Nelson AG, Kokkonen J, Arnall DA, Li L (2012) Acute stretching increases postural stability in nonbalance trained individuals. J Strength Cond Res 26:3095–3100. https://doi.org/10.1519/JSC.0b013e3182430185

    Article  PubMed  Google Scholar 

  28. Owsley C, McGwin G Jr (2010) Vision and driving. Vis Res 50:2348–2361. https://doi.org/10.1016/j.visres.2010.05.021

    Article  PubMed  Google Scholar 

  29. Patel KV, Phelan EA, Leveille SG et al (2014) High prevalence of falls, fear of falling, and impaired balance in older adults with pain in the United States: findings from the 2011 National Health and Aging Trends Study. J Am Geriatr Soc 62:1844–1852. https://doi.org/10.1111/jgs.13072

    Article  PubMed  PubMed Central  Google Scholar 

  30. Paulus WM, Straube A, Brandt T (1984) Visual stabilization of posture. Physiological stimulus characteristics and clinical aspects. Brain 107(4):1143–1163

    Article  Google Scholar 

  31. Prado JM, Stoffregen TA, Duarte M (2007) Postural sway during dual tasks in young and elderly adults. Gerontology 53:274–281. https://doi.org/10.1159/000102938

    Article  PubMed  Google Scholar 

  32. Rey F, Le TT, Bertin R, Kapoula Z (2008) Saccades horizontal or vertical at near or at far do not deteriorate postural control. Auris Nasus Larynx 35:185–191. https://doi.org/10.1016/j.anl.2007.07.001

    Article  PubMed  Google Scholar 

  33. Rodrigues ST, Aguiar SA, Polastri PF, Godoi D, Moraes R, Barela JA (2013) Effects of saccadic eye movements on postural control stabilization. Motriz 19:614–619

    Google Scholar 

  34. 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 584:292–295. https://doi.org/10.1016/j.neulet.2014.10.045

    CAS  Article  PubMed  Google Scholar 

  35. Rougier P, Garin M (2007) Performing saccadic eye movements or blinking improves postural control. Mot Control 11:213–223

    Article  Google Scholar 

  36. Schutte KH, Seerden S, Venter R, Vanwanseele B (2018) Influence of outdoor running fatigue and medial tibial stress syndrome on accelerometer-based loading and stability. Gait Posture 59:222–228. https://doi.org/10.1016/j.gaitpost.2017.10.021

    Article  PubMed  Google Scholar 

  37. Seliga R, Bhattacharya A, Succop P, Wickstrom R, Smith D, Willeke K (1991) Effect of work load and respirator wear on postural stability, heart rate, and perceived exertion. Am Ind Hyg Assoc J 52:417–422. https://doi.org/10.1080/15298669191364965

    CAS  Article  PubMed  Google Scholar 

  38. Skarabot J, Beardsley C, Stirn I (2015) Comparing the effects of self-myofascial release with static stretching on ankle range-of-motion in adolescent athletes. Int J Sports Phys Ther 10:203–212

    PubMed  PubMed Central  Google Scholar 

  39. Skinner HB, Wyatt MP, Hodgdon JA, Conard DW, Barrack RL (1986) Effect of fatigue on joint position sense of the knee. J Orthop Res 4:112–118. https://doi.org/10.1002/jor.1100040115

    CAS  Article  PubMed  Google Scholar 

  40. Stins JF, Michielsen ME, Roerdink M, Beek PJ (2009) Sway regularity reflects attentional involvement in postural control: effects of expertise, vision and cognition. Gait Posture 30:106–109. https://doi.org/10.1016/j.gaitpost.2009.04.001

    CAS  Article  PubMed  Google Scholar 

  41. Stoffregen TA, Bardy BG, Bonnet CT, Pagulayan RJ (2006) Postural stabilization of visually guided eye movements. Ecol Psychol 18:191–222. https://doi.org/10.1207/s15326969eco1803_3

    Article  Google Scholar 

  42. Stoffregen TA, Bardy BG, Bonnet CT, Hove P, Oullier O (2007) Postural sway and the frequency of horizontal eye movements. Mot Control 11:86–102

    Google Scholar 

  43. Stoffregen TA, Villard S, Yu YW (2009) Body sway at sea for two visual tasks and three stance widths. Aviat Space Environ Med 80:1039–1043. https://doi.org/10.3357/Asem.2538.2009

    Article  PubMed  Google Scholar 

  44. Strupp M, Glasauer S, Jahn K, Schneider E, Krafczyk S, Brandt T (2003) Eye movements and balance. Ann N Y Acad Sci 1004:352–358

    Article  Google Scholar 

  45. Tanaka H, Uetake T (2005) Characteristics of postural sway in older adults standing on a soft surface. J Hum Ergol (Tokyo) 34:35–40

    Google Scholar 

  46. Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol (1985) 104:542–550. https://doi.org/10.1152/japplphysiol.01053.2007

    Article  Google Scholar 

  47. Thomas KS, Magal M (2014) How does physical activity impact postural stability? J Nov Physiother 4:2

    Google Scholar 

  48. Thomas NM, Bampouras TM, Donovan T, Dewhurst S (2016) Eye movements affect postural control in young and older females. Front Aging Neurosci 8:216. https://doi.org/10.3389/fnagi.2016.00216

    Article  PubMed  PubMed Central  Google Scholar 

  49. Toledo DR, Barela JA (2010) Sensory and motor differences between young and older adults: Somatosensory contribution to postural control. Rev Bras Fisioter 14:267–275 doi. https://doi.org/10.1590/S1413-35552010000300004

    Article  PubMed  Google Scholar 

  50. Uchida Y, Demura S (2016) Differences in leg muscle activity and body sway between elderly adults able and unable to maintain one-leg stance for 1 min: the effect of hand support. Aging Clin Exp Res 28:669–677. https://doi.org/10.1007/s40520-015-0461-x

    Article  PubMed  Google Scholar 

  51. Walsh GS (2017) Effect of static and dynamic muscle stretching as part of warm up procedures on knee joint proprioception and strength. Hum Mov Sci 55:189–195. https://doi.org/10.1016/j.humov.2017.08.014

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jan M. Hondzinski.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yeomans, M.A., Nelson, A.G., MacLellan, M.J. et al. Visually-guided saccades attenuate postural sway under non-fatigued, fatigued, and stretched states. Exp Brain Res 236, 3351–3361 (2018). https://doi.org/10.1007/s00221-018-5384-2

Download citation

Keywords

  • Balance
  • Force plate
  • Physical activity
  • Sensorimotor control
  • Vision