Experimental Brain Research

, Volume 233, Issue 5, pp 1597–1606 | Cite as

High-gain visual feedback exacerbates ankle movement variability in children

  • Hwasil Moon
  • Changki Kim
  • MinHyuk Kwon
  • Yen-Ting Chen
  • Emily Fox
  • Evangelos A. ChristouEmail author
Research Article


The purpose was to compare the effect of low- and high-gain visual feedback on ankle movement variability and muscle activation in children and young adults. Six young adults (19.8 ± 0.6 years) and nine children (9.4 ± 1.6 years) traced a sinusoidal target by performing ankle plantar/dorsiflexion movements. The targeted range of motion was 10°, and the frequency of the sinusoidal target was 0.4 Hz for 35 s. Low-gain visual feedback was 0.66°, and high-gain visual feedback was 4.68°. Surface EMG was recorded from the tibialis anterior (TA) muscle. Movement variability amplitude was quantified as the standard deviation of the position fluctuations after the task frequency was removed with a notch filter (second-order; 0.3–0.5 Hz). We quantified the oscillations in movement variability and TA EMG burst using the following frequency bands: 0–0.3, 0.3–0.6, 0.6–0.9, 0.9–1.2, and 1.2–1.5 Hz. Children exhibited greater movement variability than young adults, which was exacerbated during the high-gain visual feedback condition (P < 0.05). The greater ankle movement variability in children at the high-gain visual feedback condition was predicted by greater power within the 0–0.3 Hz of their movement variability (R 2 = 0.51, P < 0.001). The greater power in movement variability from 0 to 0.3 Hz in children was predicted by greater power within the 0–0.3 Hz in their TA EMG burst activity (R 2 = 0.6, P < 0.001). The observed deficiency in movement control with amplified visual feedback in children may be related to an ineffective use of visual feedback and the immaturity of the cortico-motor systems.


Adolescence Variability EMG Lower limb 



The authors would like to thank Hannah Mora, Ericka Miller, Brittany Forster, and Mark Costanzo for their help with data collection. This study was supported by R01 AG031769 to Evangelos A. Christou.

Conflict of interest



  1. Ameratunga D, Johnston L, Burns Y (2004) Goal-directed upper limb movements by children with and without DCD: a window into perceptuo-motor dysfunction? Physiother Res Int 9:1–12CrossRefPubMedGoogle Scholar
  2. Arpin DJ, Stuberg W, Stergiou N, Kurz MJ (2013) Motor control of the lower extremity musculature in children with cerebral palsy. Res Dev Disabil 34:1134–1143. doi: 10.1016/j.ridd.2012.12.014 CrossRefPubMedGoogle Scholar
  3. Berlin L, Bohlin G, Rydell AM (2003) Relations between inhibition, executive functioning, and ADHD symptoms: a longitudinal study from age 5 to 8(1/2) years. Child Neuropsychol 9:255–266. doi: 10.1076/chin. CrossRefPubMedGoogle Scholar
  4. Calvin WH, Stevens CF (1968) Synaptic noise and other sources of randomness in motoneuron interspike intervals. J Neurophysiol 31:574–587PubMedGoogle Scholar
  5. Christou EA, Jakobi JM, Critchlow A, Fleshner M, Enoka RM (2004) The 1- to 2-Hz oscillations in muscle force are exacerbated by stress, especially in older adults. J Appl Physiol (1985) 97:225–235. doi: 10.1152/japplphysiol.00066.2004 CrossRefGoogle Scholar
  6. Christou EA, Moon H, Kim C et al (2014) Force variability is related to low-frequency oscillations in force and EMG burst: 2487: Board# 192 May 30 9:30 AM–11:00 AM. Med Sci Sports Exerc 46:519Google Scholar
  7. Cleary KM, Donkers FC, Evans AM, Belger A (2013) Investigating developmental changes in sensory processing: visual mismatch response in healthy children. Front Hum Neurosci 30(7):922. doi: 10.3389/fnhum.2013.00922 Google Scholar
  8. Coombes SA, Corcos DM, Sprute L, Vaillancourt DE (2010) Selective regions of the visuomotor system are related to gain-induced changes in force error. J Neurophysiol 103:2114–2123. doi: 10.1152/jn.00920.2009 CrossRefPubMedCentralPubMedGoogle Scholar
  9. Deutsch KM, Newell KM (2001) Age differences in noise and variability of isometric force production. J Exp Child Psychol 80:392–408. doi: 10.1006/jecp.2001.2642 CrossRefPubMedGoogle Scholar
  10. Deutsch KM, Newell KM (2002) Children’s coordination of force output in a pinch grip task. Dev Psychobiol 41:253–264. doi: 10.1002/dev.10051 CrossRefPubMedGoogle Scholar
  11. Deutsch KM, Newell KM (2006) Age-related changes in the frequency profile of children’s finger tremor. Neurosci Lett 404:191–195. doi: 10.1016/j.neulet.2006.05.047 CrossRefPubMedGoogle Scholar
  12. Dye MW, Bavelier D (2010) Differential development of visual attention skills in school-age children. Vis Res 50:452–459. doi: 10.1016/j.visres.2009.10.010 CrossRefPubMedCentralPubMedGoogle Scholar
  13. Eiland L, Romeo RD (2013) Stress and the developing adolescent brain. Neuroscience 249:162–171. doi: 10.1016/j.neuroscience.2012.10.048 CrossRefPubMedCentralPubMedGoogle Scholar
  14. Elias LJ, Bryden MP (1998) Footedness is a better predictor of language lateralisation than handedness. Laterality 3:41–51. doi: 10.1080/713754287 PubMedGoogle Scholar
  15. Elliott D, Hansen S, Grierson LE, Lyons J, Bennett SJ, Hayes SJ (2010) Goal-directed aiming: two components but multiple processes. Psychol Bull 136:1023–1044. doi: 10.1037/a0020958 CrossRefPubMedGoogle Scholar
  16. Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, Tracy BL (2003) Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 13:1–12CrossRefPubMedGoogle Scholar
  17. Fox EJ, Baweja HS, Kim C, Kennedy DM, Vaillancourt DE, Christou EA (2013) Modulation of force below 1 Hz: age-associated differences and the effect of magnified visual feedback. PLoS One 8:e55970. doi: 10.1371/journal.pone.0055970 CrossRefPubMedCentralPubMedGoogle Scholar
  18. Fox EJ, Moon H, Kwon M, Chen YT, Christou EA (2014) Neuromuscular control of goal-directed ankle movements differs for healthy children and adults. Eur J Appl Physiol. doi: 10.1007/s00421-014-2915-9 PubMedGoogle Scholar
  19. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374CrossRefPubMedGoogle Scholar
  20. Liu R, Zhou J, Zhao H, Dai Y, Zhang Y, Tang Y, Zhou Y (2014) Immature visual neural system in children reflected by contrast sensitivity with adaptive optics correction. Sci Rep 4:4687. doi: 10.1038/srep04687 PubMedCentralPubMedGoogle Scholar
  21. Lodha N, Misra G, Coombes SA, Christou EA, Cauraugh JH (2013) Increased force variability in chronic stroke: contributions of force modulation below 1 Hz. PLoS One 8:e83468. doi: 10.1371/journal.pone.0083468 CrossRefPubMedCentralPubMedGoogle Scholar
  22. Martinez-Roda JA, Vilaseca M, Ondategui JC, Giner A, Burgos FJ, Cardona G, Pujol J (2011) Optical quality and intraocular scattering in a healthy young population. Clin Exp Optom 94:223–229. doi: 10.1111/j.1444-0938.2010.00535.x CrossRefPubMedGoogle Scholar
  23. Matthews PB (1996) Relationship of firing intervals of human motor units to the trajectory of post-spike after-hyperpolarization and synaptic noise. J Physiol 492(Pt 2):597–628CrossRefPubMedCentralPubMedGoogle Scholar
  24. Michael R, Guevara O, de la Paz M, Alvarez de Toledo J, Barraquer RI (2011) Neural contrast sensitivity calculated from measured total contrast sensitivity and modulation transfer function. Acta Ophthalmol 89:278–283. doi: 10.1111/j.1755-3768.2009.01665.x CrossRefPubMedGoogle Scholar
  25. Moon H, Kim C, Kwon M, Chen Y, Fox EJ, Christou EA (2013) Altered oscillations in EMG variability explain impaired ankle movement control in children during a high-gain visual feedback condition. In: Society for Neuroscience, vol 263.11/QQ17, San Diego, CAGoogle Scholar
  26. Moon H, Kim C, Kwon M, Chen Y, Onushko T, Lodha N, Christou EA (2014) Force control is related to low-frequency oscillations in force and surface EMG. PLoS One 9(11):e109202CrossRefPubMedCentralPubMedGoogle Scholar
  27. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  28. Schmied A, Pagni S, Sturm H, Vedel JP (2000) Selective enhancement of motoneurone short-term synchrony during an attention-demanding task. Exp Brain Res 133:377–390CrossRefPubMedGoogle Scholar
  29. Takahashi CD, Nemet D, Rose-Gottron CM, Larson JK, Cooper DM, Reinkensmeyer DJ (2003) Neuromotor noise limits motor performance, but not motor adaptation, in children. J Neurophysiol 90:703–711. doi: 10.1152/jn.01173.2002 CrossRefPubMedGoogle Scholar
  30. Taylor AM, Enoka RM (2004) Optimization of input patterns and neuronal properties to evoke motor neuron synchronization. J Comput Neurosci 16:139–157. doi: 10.1023/B:JCNS.0000014107.16610.2e CrossRefPubMedGoogle Scholar
  31. Taylor AM, Christou EA, Enoka RM (2003) Multiple features of motor-unit activity influence force fluctuations during isometric contractions. J Neurophysiol 90:1350–1361. doi: 10.1152/jn.00056.2003 CrossRefPubMedGoogle Scholar
  32. Yan JH, Thomas JR (2002) Arm movement control: differences between children with and without attention deficit hyperactivity disorder. Res Q Exerc Sport 73:10–18CrossRefPubMedGoogle Scholar
  33. Yan JH, Thomas JR, Stelmach GE, Thomas KT (2000) Developmental features of rapid aiming arm movements across the lifespan. J Mot Behav 32:121–140. doi: 10.1080/00222890009601365 CrossRefPubMedGoogle Scholar
  34. Yan JH, Thomas KT, Stelmach GE, Thomas JR (2003) Developmental differences in children’s ballistic aiming movements of the arm. Percept Mot Skills 96:589–598CrossRefPubMedGoogle Scholar
  35. Yoshitake Y, Shinohara M (2013a) Low-frequency component of rectified EMG is temporally correlated with force and instantaneous rate of force fluctuations during steady contractions. Muscle Nerve 47:577–584. doi: 10.1002/mus.23628 CrossRefPubMedGoogle Scholar
  36. Yoshitake Y, Shinohara M (2013b) Oscillations in motor unit discharge are reflected in the low-frequency component of rectified surface EMG and the rate of change in force. Exp Brain Res 231:267–276. doi: 10.1007/s00221-013-3689-8 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Hwasil Moon
    • 1
  • Changki Kim
    • 1
  • MinHyuk Kwon
    • 1
  • Yen-Ting Chen
    • 1
  • Emily Fox
    • 2
    • 3
  • Evangelos A. Christou
    • 1
    • 2
    Email author
  1. 1.Department of Applied Physiology and KinesiologyUniversity of FloridaGainesvilleUSA
  2. 2.Department of Physical TherapyUniversity of FloridaGainesvilleUSA
  3. 3.Brooks RehabilitationJacksonvilleUSA

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