Sensory Reweighting During Bipedal Quiet Standing in Adolescents

Click name to view affiliation

Alberto Pardo-Ibáñez Universidad de Valencia

Search for other papers by Alberto Pardo-Ibáñez in
Current site
Google Scholar
PubMed
Close
*
,
Jose L. Bermejo Universidad de Valencia

Search for other papers by Jose L. Bermejo in
Current site
Google Scholar
PubMed
Close
*
,
Sergio Gandia Universidad de Valencia

Search for other papers by Sergio Gandia in
Current site
Google Scholar
PubMed
Close
*
,
Julien Maitre Université de Pau et des Pays de l’Adour

Search for other papers by Julien Maitre in
Current site
Google Scholar
PubMed
Close
*
,
Israel Villarrasa-Sapiña Universidad de Valencia

Search for other papers by Israel Villarrasa-Sapiña in
Current site
Google Scholar
PubMed
Close
*
,
Isaac Estevan Universidad de Valencia

Search for other papers by Isaac Estevan in
Current site
Google Scholar
PubMed
Close
*
, and
Xavier Garcia-Masso Universidad de Valencia

Search for other papers by Xavier Garcia-Masso in
Current site
Google Scholar
PubMed
Close
*
Restricted access

A cross-sectional, prospective, between-subjects design was used in this study to establish the differences in sensory reweighting of postural control among different ages during adolescence. A total of 153 adolescents (five age groups; 13–17 years old) performed bipedal standing in three sensory conditions (i.e., with visual restriction, vestibular disturbance, and proprioceptive disturbance). Center of pressure displacement signals were measured in mediolateral and anteroposterior directions to characterize reweighting in the sensory system in static postural control when sensory information is disturbed or restricted during adolescent growth. The results indicate a development of postural control, showing large differences between subjects of 13–14 years old and older adolescents. A critical change was found in sensory reweighting during bipedal stance with disturbance of proprioceptive information at 15 years old. Adolescents of 13–14 years old showed less postural control and performance than older adolescents during the disturbance of proprioceptive information. Moreover, the results demonstrated that the visual system achieves its development around 15–16 years old. In conclusion, this research suggests that a difference of sensory reweighting under this type of sensorial condition and sensory reweight systems would seem to achieve stabilization at the age of 15.

Pardo-Ibáñez, Bermejo, Gandia, and Villarrasa-Sapiña are with the Departamento de Educación Física y Deportiva, Universidad de Valencia, Valencia, Spain. Villarrasa-Sapiña is also with Universidad Internacional de la Rioja (UNIR). Maitre is with Laboratoire Mouvement, Equilibre, Performance et Santé (MEPS, EA 4445), Université de Pau et des Pays de l’Adour, Tarbes, France. Estevan and Garcia-Masso are with the Departamento de Didáctica de la Expresión Musical, Plástica y Corporal, Universidad de Valencia, Valencia, Spain.

Garcia-Masso (xavier.garcia@uv.es) is corresponding author.
  • Collapse
  • Expand
  • Ajrezo, L., Wiener-Vacher, S., & Bucci, M.P. (2013). Saccades improve postural control: A developmental study in normal children. PLoS One, 8(11), e81066. PubMed ID: 24278379 doi:10.1371/journal.pone.0081066

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Assaiante, C., & Amblard, B. (1995). An ontogenetic model for the sensorimotor organization of balance control in humans. Human Movement Science, 14(1), 1343. doi:10.1016/0167-9457(94)00048-J

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Barela, A.M.F., Barela, J.A., Rinaldi, N.M., & de Toledo, D.R. (2009). Influence of imposed optic flow characteristics and intention on postural responses. Motor Control, 13(2), 119129. PubMed ID: 19454775 doi:10.1123/mcj.13.2.119

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Barozzi, S., Socci, M., Soi, D., Di Berardino, F., Fabio, G., Forti, S., … Cesarani, A. (2014). Reliability of postural control measures in children and young adolescents. European Archives of Oto-Rhino-Laryngology: Official Journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS), 271(7), 20692077. doi:10.1007/s00405-014-2930-9

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Billot, M., Handrigan, G.A., Simoneau, M., & Teasdale, N. (2015). Reduced plantar sole sensitivity induces balance control modifications to compensate ankle tendon vibration and vision deprivation. Journal of Electromyography and Kinesiology, 25(1), 155160. PubMed ID: 24993669 doi:10.1016/j.jelekin.2014.06.003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bordoni, B., & Daly, D.T. (2019). Neuroanatomy, cranial nerve 8 (vestibulocochlear). In StatPearls [Internet]. StatPearls Publishing. https://www.statpearls.com/sp/ph/197/19673/

    • Search Google Scholar
    • Export Citation
  • Borel, L., & Ribot-Ciscar, E. (2016). Improving postural control by applying mechanical noise to ankle muscle tendons. Experimental Brain Research, 234(8), 23052314. PubMed ID: 27021075 doi:10.1007/s00221-016-4636-2

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Brumagne, S., Cordo, P., & Verschueren, S. (2004). Proprioceptive weighting changes in persons with low back pain and elderly persons during upright standing. Neuroscience Letters, 366(1), 6366. PubMed ID: 15265591 doi:10.1016/j.neulet.2004.05.013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ceyte, H., Cian, C., Zory, R., Barraud, P.-A., Roux, A., & Guerraz, M. (2007). Effect of Achilles tendon vibration on postural orientation. Neuroscience Letters, 416(1), 7175. PubMed ID: 17300868 doi:10.1016/j.neulet.2007.01.044

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Clark, R.A., Bryant, A.L., Pua, Y., McCrory, P., Bennell, K., & Hunt, M. (2010). Validity and reliability of the Nintendo Wii Balance Board for assessment of standing balance. Gait & Posture, 31(3), 307310. PubMed ID: 20005112 doi:10.1016/j.gaitpost.2009.11.012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Cuisinier, R., Olivier, I., Vaugoyeau, M., Nougier, V., & Assaiante, C. (2011). Reweighting of sensory inputs to control quiet standing in children from 7 to 11 and in adults. PLoS One, 6(5), e19697. PubMed ID: 21573028 doi:10.1371/journal.pone.0019697

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Faigenbaum, A.D., Myer, G.D., Fernandez, I.P., Carrasco, E.G., Bates, N., Farrell, A., … Kang, J. (2014). Feasibility and reliability of dynamic postural control measures in children in first through fifth grades. International Journal of Sports Physical Therapy, 9(2), 140148. PubMed ID: 24790775

    • Search Google Scholar
    • Export Citation
  • Gandemer, L., Parseihian, G., Kronland-Martinet, R., & Bourdin, C. (2014). The influence of horizontally rotating sound on standing balance. Experimental Brain Research, 232(12), 38133820. PubMed ID: 25146572 doi:10.1007/s00221-014-4066-y

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Godoi, D., & Barela, J.A. (2008). Body sway and sensory motor coupling adaptation in children: Effects of distance manipulation. Developmental Psychobiology, 50(1), 7787. PubMed ID: 18085560 doi:10.1002/dev.20272

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Golz, A., Westerman, S.T., Westerman, L.M., Goldenberg, D., Netzer, A., Wiedmyer, T., … Joachims, H.Z. (2001). The effects of noise on the vestibular system. American Journal of Otolaryngology, 22(3), 190196. PubMed ID: 11351289 doi:10.1053/ajot.2001.23428

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Groselj, J., Osredkar, D., Sember, V., & Pajek, M. (2019). Associations between balance and other fundamental motor skills in pre-adolescents. Medicina Dello Sport, 72(2), 200215. doi:10.23736/S0025-7826.19.03482-3s

    • Search Google Scholar
    • Export Citation
  • Hatzitaki, V., Zisi, V., Kollias, I., & Kioumourtzoglou, E. (2002). Perceptual-motor contributions to static and dynamic balance control in children. Journal of Motor Behavior, 34(2), 161170. PubMed ID: 12057889 doi:10.1080/00222890209601938

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hirabayashi, S., & Iwasaki, Y. (1995). Developmental perspective of sensory organization on postural control. Brain & Development, 17(2), 111113. PubMed ID: 7542846 doi:10.1016/0387-7604(95)00009-Z

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Jeka, J., Oie, K.S., & Kiemel, T. (2000). Multisensory information for human postural control: Integrating touch and vision. Experimental Brain Research, 134(1), 107125. PubMed ID: 11026732 doi:10.1007/s002210000412

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Larsen, L.R., Jørgensen, M.G., Junge, T., Juul-Kristensen, B., & Wedderkopp, N. (2014). Field assessment of balance in 10 to 14 year old children, reproducibility and validity of the Nintendo Wii board. BMC Pediatrics, 14, 144. PubMed ID: 24913461 doi:10.1186/1471-2431-14-144

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lee, D.N., & Aronson, E. (1974). Visual proprioceptive control of standing in human infants. Perception & Psychophysics, 15(3), 529532. doi:10.3758/BF03199297

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lishman, J.R., & Lee, D.N. (1973). The autonomy of visual kinaesthesis. Perception, 2(3), 287294. PubMed ID: 4546578 doi:10.1068/p020287

  • Mahboobin, A., Loughlin, P.J., Redfern, M.S., Anderson, S.O., Atkeson, C.G., & Hodgins, J.K. (2008). Sensory adaptation in human balance control: Lessons for biomimetic robotic bipeds. Neural Networks: The Official Journal of the International Neural Network Society, 21(4), 621627. doi:10.1016/j.neunet.2008.03.013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mahboobin, A., Loughlin, P.J., Redfern, M.S., & Sparto, P.J. (2005). Sensory re-weighting in human postural control during moving-scene perturbations. Experimental Brain Research, 167(2), 260267. PubMed ID: 16025292 doi:10.1007/s00221-005-0053-7

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Maitre, J., & Paillard, T. (2016). Postural effects of vestibular manipulation depend on the physical activity status. PLoS One, 11(9), e0162966. PubMed ID: 27627441 doi:10.1371/journal.pone.0162966

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Micarelli, A., Viziano, A., Augimeri, I., Micarelli, B., & Alessandrini, M. (2019). Age-related assessment of postural control development: A cross-sectional study in children and adolescents. Journal of Motor Behavior. (Advance online publication). doi:10.1080/00222895.2019.1643284

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nashner, L.M. (1993). Practical biomechanics and physiology of balance. In G.P. Jacobson, C.W. Newman, & J.M. Kartush (Eds.), Handbook of balance function testing (pp. 261279). St Louis, MO: Mosby Year Book.

    • Search Google Scholar
    • Export Citation
  • Oie, K.S., Kiemel, T., & Jeka, J.J. (2002). Multisensory fusion: Simultaneous re-weighting of vision and touch for the control of human posture. Cognitive Brain Research, 14(1), 164176. PubMed ID: 12063140 doi:10.1016/S0926-6410(02)00071-X

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Onambele, G.L., Narici, M.V., & Maganaris, C.N. (2006). Calf muscle-tendon properties and postural balance in old age. Journal of Applied Physiology, 100(6), 20482056. doi:10.1152/japplphysiol.01442.2005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Paillard, T., & Noé, F. (2015). Techniques and methods for testing the postural function in healthy and pathological subjects. BioMed Research International, 2015, 891390. PubMed ID: 26640800 doi:10.1155/2015/891390

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Park, D.-S., & Lee, G. (2014). Validity and reliability of balance assessment software using the Nintendo Wii balance board: Usability and validation. Journal of Neuroengineering and Rehabilitation, 11, 99. PubMed ID: 24912769 doi:10.1186/1743-0003-11-99

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Park, S.H., Lee, K., Lockhart, T., & Kim, S. (2011). Effects of sound on postural stability during quiet standing. Journal of Neuroengineering and Rehabilitation, 8(1) 67. PubMed ID: 22168248 doi:10.1186/1743-0003-8-67

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Peterka, R.J., & Black, F.O. (1990). Age-related changes in human posture control: Motor coordination tests. Journal of Vestibular Research, 1(1), 8796. PubMed ID: 1670140

    • Search Google Scholar
    • Export Citation
  • Peterka, R.J., & Loughlin, P.J. (2004). Dynamic regulation of sensorimotor integration in human postural control. Journal of Neurophysiology, 91(1), 410423. PubMed ID: 13679407 doi:10.1152/jn.00516.2003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Peterson, M.L., Christou, E., & Rosengren, K.S. (2006). Children achieve adult-like sensory integration during stance at 12-years-old. Gait & Posture, 23(4), 455463. PubMed ID: 16002294 doi:10.1016/j.gaitpost.2005.05.003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Polastri, P.F., & Barela, J.A. (2013). Adaptive visual re-weighting in children’s postural control. PLoS One, 8(12), e82215. PubMed ID: 24324766 doi:10.1371/journal.pone.0082215

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Prieto, T.E., Myklebust, J.B., Hoffmann, R.G., Lovett, E.G., & Myklebust, B.M. (1996). Measures of postural steadiness: Differences between healthy young and elderly adults. IEEE Transactions on Biomedical Engineering, 43(9), 956966. PubMed ID: 9214811 doi:10.1109/10.532130

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Raymakers, J.A., Samson, M.M., & Verhaar, H.J.J. (2005). The assessment of body sway and the choice of the stability parameter(s). Gait & Posture, 21(1), 4858. PubMed ID: 15536033 doi:10.1016/j.gaitpost.2003.11.006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Riach, C.L., & Hayes, K.C. (1987). Maturation of postural sway in young children. Developmental Medicine & Child Neurology, 29(5), 650658. PubMed ID: 3666328 doi:10.1111/j.1469-8749.1987.tb08507.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rival, C., Ceyte, H., & Olivier, I. (2005). Developmental changes of static standing balance in children. Neuroscience Letters, 376(2), 133136. PubMed ID: 15698935 doi:10.1016/j.neulet.2004.11.042

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sparto, P.J., Redfern, M.S., Jasko, J.G., Casselbrant, M.L., Mandel, E.M., & Furman, J.M. (2006). The influence of dynamic visual cues for postural control in children aged 7–12 years. Experimental Brain Research, 168(4), 505516. PubMed ID: 16151780 doi:10.1007/s00221-005-0109-8

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tanaka, T., Kojima, S., Takeda, H., Ino, S., & Ifukube, T. (2001). The influence of moving auditory stimuli on standing balance in healthy young adults and the elderly. Ergonomics, 44(15), 14031412. PubMed ID: 11936831 doi:10.1080/00140130110110601

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thompson, C., Bélanger, M., & Fung, J. (2007). Effects of bilateral Achilles tendon vibration on postural orientation and balance during standing. Clinical Neurophysiology, 118(11), 24562467. PubMed ID: 17897877 doi:10.1016/j.clinph.2007.08.013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • van der Kooij, H., Jacobs, R., Koopman, B., & van der Helm, F. (2001). An adaptive model of sensory integration in a dynamic environment applied to human stance control. Biological Cybernetics, 84(2), 103115. PubMed ID: 11205347 doi:10.1007/s004220000196

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Welgampola, M.S., & Colebatch, J.G. (2001). Vestibulospinal reflexes: Quantitative effects of sensory feedback and postural task. Experimental Brain Research, 139(3), 345353. PubMed ID: 11545473 doi:10.1007/s002210100754

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Woollacott, M., Debu, B., & Mowatt, M. (1987). Neuromuscular control of posture in the infant and child: Is vision dominant? Journal of Motor Behavior, 19(2), 167186. PubMed ID: 14988057 doi:10.1080/00222895.1987.10735406

    • Crossref
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 2614 508 32
Full Text Views 58 38 5
PDF Downloads 27 3 0