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Muscle synergies underlying control of taking a step during support surface translation

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European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

We investigated the muscle activation patterns and the center of pressure (COP) displacement in stepping behavior to determine the relations between anticipatory synergy adjustments (ASAs) and anticipatory postural adjustments (APAs) during support surface translation.

Methods

Surface muscle activity of eleven leg and trunk muscles was analyzed to identify sets of four muscle modes (M-modes). Linear combination of M-modes and their relationship to changes in the COP shift in the anterior–posterior (AP) direction were then determined. Uncontrolled manifold (UCM) analysis was performed to determine variance components in the M-mode space and indices of M-mode synergy stabilizing the COP shift.

Results

Prior to the step initiation, synergies stabilizing COP were seen in both conditions. The synergy index started to drop before a change in the averaged activation levels across trials in postural muscles. The magnitude of synergy index was significantly larger under the perturbation condition.

Conclusions

Results of the study have revealed that the central nervous system is able to prepare multi-muscle synergies when a step is performed during support surface translation. Prior to APAs, ASAs reduce stability of COPAP coordinate that is to be adjusted during the APAs. These findings may help get closer to understanding of physiological mechanism of postural preparation to external perturbation.

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Abbreviations

AP:

Anterior–posterior

APAs:

Anticipatory postural adjustments

ASAs:

Anticipatory synergy adjustments

BF:

Biceps femoris

COP:

Center of pressure

ES:

Erector spinae

GL:

Lateral head of gastrocnemius

GM:

Medial head of gastrocnemius

PCA:

Principal component analysis

RA:

Rectus abdominis

RF:

Rectus femoris

SOL:

Soleus

ST:

Semitendinosus

TA:

Tibialis anterior

UCM:

Uncontrolled manifold

VL:

Vastus lateralis

VM:

Vastus medialis

References

  • Asaka T, Wang Y, Fukushima J, Latash ML (2008) Learning effects on muscle modes and multi-mode postural synergies. Exp Brain Res 184(3):323–338

    Article  PubMed  PubMed Central  Google Scholar 

  • Belen’kii VE, Gurfinkel VS, Pal’tsev EI (1967) Control elements of voluntary movements. Biofizika 12(1):135–141

    PubMed  Google Scholar 

  • Bernstein NA (1967) The coordination and regulation of movements. Pergamon, London

    Google Scholar 

  • Bertucco M, Cesari P, Latash ML (2013) Fitts’ law in early postural adjustment. Neuroscience 231:61–69

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chvatal SA, Torres-Oviedo G, Safavynia SA, Ting LH (2011) Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors. J Neurophysiol 106(2):999–1015

    Article  PubMed  PubMed Central  Google Scholar 

  • Couillandre A, Maton B, Breniere Y (2002) Voluntary toe-walking gait initiation: electromyographical and biomechanical aspects. Exp Brain Res 147:313–321

    Article  PubMed  Google Scholar 

  • d’Avella A, Saltiel P, Bizzi E (2003) Combinations of muscle synergies in the construction of a natural motor behavior. Nat Neurosci 6:300–308

  • Elble RJ, Moody C, Leffler K, Sinha R (1994) The initiation of normal walking. Mov Disord 9:139–146

    Article  PubMed  CAS  Google Scholar 

  • Halliday SE, Winter DA, Frank JS, Patla AE, Prince F (1998) The initiation of gait in young, elderly, and Parkinson’s disease subjects. Gait Posture 8(1):8–14

    Article  PubMed  Google Scholar 

  • Horak FB, Nashner LM (1986) Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 55(6):1369–1381

    PubMed  CAS  Google Scholar 

  • Ito T, Azuma T, Yamashita N (2003) Anticipatory control in the initiation of a single step under biomechanical constraints in humans. Neurosci Lett 352(3):207–210

    Article  PubMed  CAS  Google Scholar 

  • Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556:267–282

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F (2005) Coordination of locomotion with voluntary movements in humans. J Neurosci 25:7238–7253

    Article  PubMed  CAS  Google Scholar 

  • Klous M, Mikulic P, Latash ML (2011) Two aspects of feed-forward postural control: anticipatory postural adjustments and anticipatory synergy adjustments. J Neurophysiol 105(5):2275–2288

    Article  PubMed  PubMed Central  Google Scholar 

  • Klous M, Mikulic P, Latash ML (2012) Early postural adjustments in preparation to whole-body voluntary sway. J Electromyogr 22(1):110–116

    Article  Google Scholar 

  • Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2004) Muscle modes during shifts of the center of pressure by standing persons: effect of instability and additional support. Exp Brain Res 157(1):18–31

    Article  PubMed  Google Scholar 

  • Krishnan V, Aruin AS, Latash ML (2011) Two stages and three components of the postural preparation to action. Exp Brain Res 212(1):47–63

    Article  PubMed  PubMed Central  Google Scholar 

  • Krishnan V, Latash ML, Aruin AS (2012) Early and late components of feed-forward postural adjustments to predictable perturbations. Clin Neurophysiol 123:1016–1026

    Article  PubMed  PubMed Central  Google Scholar 

  • Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14(3):294–322

    Google Scholar 

  • Lepers R, Breniere Y (1995) The role of anticipatory postural adjustments and gravity in gait initiation. Exp Brain Res 107(1):118–124

    Article  PubMed  CAS  Google Scholar 

  • Mattos D, Latash ML, Park E, Kuhl J, Scholz JP (2011) Unpredictable elbow joint perturbation during reaching results in multijoint motor equivalence. J Neurophysiol 106(3):1424–1436

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mille ML, Rogers MW, Martinez K, Hedman LD, Johnson ME, Lord SR, Fitzpatrick RC (2003) Thresholds for inducing protective stepping responses to external perturbations of human standing. J Neurophysiol 90(2):666–674

    Article  PubMed  Google Scholar 

  • Mohapatra S, Kukkar KK, Aruin AS (2014) Support surface related changes in feedforward and feedback control of standing posture. J Electromyogr Kinesiol 24(1):144–152

    Article  PubMed  PubMed Central  Google Scholar 

  • Nachshon I, Denno D, Aurand S (1983) Lateral preference of hand, eye and foot: relation to cerebral dominance. Int J Neurosci 18(1–2):1–9

    Article  PubMed  CAS  Google Scholar 

  • Robert T, Zatsiorsky VM, Latash ML (2008) Multi-muscle synergies in an unusual postural task: quick shear force production. Exp Brain Res 187(2):237–253

    Article  PubMed  PubMed Central  Google Scholar 

  • Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306

    Article  PubMed  CAS  Google Scholar 

  • Schöner G (1995) Recent developments and problems in human movement science and their conceptual implications. Ecol Psychol 8:291–314

    Article  Google Scholar 

  • Ting LH (2007) Dimensional reduction in sensorimotor systems: a framework for understanding muscle coordination of posture. Prog Brain Res 165:299–321

    Article  PubMed  PubMed Central  Google Scholar 

  • Torres-Oviedo G, Ting LH (2007) Muscle synergies characterizing human postural responses. J Neurophysiol 98(4):2144–2156

    Article  PubMed  Google Scholar 

  • Torres-Oviedo G, Macpherson JM, Ting LH (2006) Muscle synergy organization is robust across a variety of postural perturbations. J Neurophysiol 96(3):1530–1546

    Article  PubMed  Google Scholar 

  • Wang Y, Asaka T (2008) Muscle synergies involved in shifts of the center of pressure while standing on a narrow support. Brain Res Bull 76(1–2):16–25

    Article  PubMed  Google Scholar 

  • Wang Y, Zatsiorsky VM, Latash ML (2005) Muscle synergies involved in shifting the center of pressure while making a first step. Exp Brain Res 167(2):196–210

    Article  PubMed  Google Scholar 

  • Wang Y, Asaka T, Zatsiorsky VM, Latash ML (2006a) Muscle synergies during voluntary body sway: combining across-trials and within-a-trial analyses. Exp Brain Res 174(4):679–693

    Article  PubMed  Google Scholar 

  • Wang Y, Zatsiorsky VM, Latash ML (2006b) Muscle synergies involved in preparation to a step made under the self-paced and reaction time instructions. Clin Neurophysiol 117:41–56

    Article  PubMed  Google Scholar 

  • Wang Y, Kenyon RV, Keshner EA (2010) Identifying the control of physically and perceptually evoked sway responses with coincident visual scene velocities and tilt of the base of support. Exp Brain Res 201(4):663–672

    Article  PubMed  Google Scholar 

  • Wang Y, Asaka T, Watanabe K (2013) Multi-muscle synergies in elderly individuals: preparation to a step made under the self-paced and reaction time instructions. Exp Brain Res 226(4):463–472

    Article  PubMed  Google Scholar 

  • Wang Y, Watanabe K, Asaka T, Wan FT (2014) Muscle synergies in preparation to a step made with and without obstacle. Eur J Appl Physiol 114(12):2561–2569

    Article  PubMed  Google Scholar 

  • Wang Y, Watanabe K, Asaka T (2015a) Muscle synergies in preparation to a step made with obstacle in elderly individuals. J Neuroeng Rehabil 12:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Watanabe K, Asaka T (2015b) Age effects on multi-muscle modes during voluntary body sway. Res Sports Med 23(1):88–101

    Article  PubMed  Google Scholar 

  • Winter DA, Prince F, Frank JS, Powell C, Zabjek KF (1996) Unified theory regarding A/P and M/L balance in quiet stance. J Neurophysiol 75:2334–2343

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China [grant #31371207] and the Natural Science Foundation of Tianjin [grant #14JCYBJC43300]. We thank Zhuoyue Zhao and Cuixia Gu for their assistance in the data collection.

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Authors and Affiliations

  1. Tianjin Key Lab of Exercise Physiology and Sports Medicine, Department of Health and Exercise Science, Tianjin University of Sport, 51 Weijin South Street, Hexi District, Tianjin, 300381, China

    Yun Wang

  2. Institute of Sports and Health Science, 3-10-31, Kagamiyama, Higashi-hiroshima, Hiroshima, 739-0046, Japan

    Kazuhiko Watanabe

  3. Department of Rehabilitation Science, Faculty of Health Sciences, Hokkaido University, N12-W5, Kita-ku, Sapporo, 060-0826, Japan

    Tadayoshi Asaka

Authors
  1. Yun Wang
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  2. Kazuhiko Watanabe
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  3. Tadayoshi Asaka
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Corresponding author

Correspondence to Yun Wang.

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The authors declare that they have no competing interests.

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Communicated by Fausto Baldissera.

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Wang, Y., Watanabe, K. & Asaka, T. Muscle synergies underlying control of taking a step during support surface translation. Eur J Appl Physiol 116, 301–309 (2016). https://doi.org/10.1007/s00421-015-3282-x

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  • DOI: https://doi.org/10.1007/s00421-015-3282-x

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