Experimental Brain Research

, Volume 210, Issue 1, pp 153–163 | Cite as

Feedforward postural muscle modes and multi-mode coordination in mild cerebellar ataxia

  • Tadayoshi Asaka
  • Yun Wang
Research Article


The purpose of this study was to investigate postural muscle synergies (M-modes) and quantitative multi-mode coordination to ensure reproducible center of pressure (COP) in anterior–posterior trajectories associated with voluntary-induced perturbations in patients with mild cerebellar ataxia. We applied the framework of the uncontrolled manifold hypothesis for the patients with ataxia. Nine patients diagnosed with spinocerebellar degeneration (SCD) and nine healthy adults stood on a force plate performed the voluntary unloading task. Ground reaction forces and surface electromyogram signals of ten trunk and leg muscles were recorded. Total variance of the first three principal components in the SCD group was similar to the control group. The co-contraction M-modes, uniting muscle pairs with opposing actions at major leg joints, were observed more frequently in the SCD group than in the control group during anticipatory postural adjustments. The quantitative multi-mode coordinations to ensure stable COP trajectories prior to and after motor actions were smaller in the SCD group than in the control group. We conclude that individuals with mild cerebellar ataxia organize feedforward muscle modes and show more co-contraction modes and impaired coordination during feedback and feedforward postural control.


Posture Cerebellar ataxia Muscle modes Coordination Electromyogram 



This work was supported in part by the Japanese Ministry of Education and Science (18500394 and 20700474). The authors are grateful to T. Kikumoto PT and K. Ikoma Dr. for their help during the experiments.


  1. Asaka T, Wang Y (2008) Effects of aging on feed forward postural synergies. J Human Kinet 20:63–70CrossRefGoogle Scholar
  2. Asaka T, Wang Y, Fukushima J, Latash ML (2008) Learning effects on muscle modes and multi-mode postural synergies. Exp Brain Res 184:323–338PubMedCrossRefGoogle Scholar
  3. Bakker M, Allum JH, Visser JE, Grüneberg C, van de Warrenburg BP, Kremer HP, Bloem BR (2006) Postural responses to multidirectional stance perturbations in cerebellar ataxia. Exp Neurol 202:21–35PubMedCrossRefGoogle Scholar
  4. Bastian AJ (2006) Learning to predict the future: the cerebellum adapts feed forward movement control. Curr Opin Neurobiol 16:645–649PubMedCrossRefGoogle Scholar
  5. Bernstein N (1967) The coordination and regulation of movements. Pergamon Press, LondonGoogle Scholar
  6. Carpenter MG, Frank JS, Silcher CP, Peysar GW (2001) The influence of postural threat on the control of upright stance. Exp Brain Res 138:210–218PubMedCrossRefGoogle Scholar
  7. Danna-Dos-Santos A, Slomka K, Zatsiorsky VM, Latash ML (2007) Muscle modes and synergies during voluntary body sway. Exp Brain Res 179:533–550PubMedCrossRefGoogle Scholar
  8. Diedrichsen J, Verstynen T, Lehman SL, Ivry RB (2005) Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol 93:801–812PubMedCrossRefGoogle Scholar
  9. Diedrichsen J, Shadmehr R, Ivry RB (2010) The coordination of movement: optimal feedback control and beyond. Trends Cogn Sci 14:31–39PubMedCrossRefGoogle Scholar
  10. Diener HC, Dichgans J, Guschlbauner B, Bacher M, Rapp H, Klockgether T (1992) The coordination of posture and voluntary movement in patients with cerebellar dysfunction. Mov Disord 7:14–22PubMedCrossRefGoogle Scholar
  11. Hair JF, Anderson RE, Tatham RL, Black WC (1995) Factor analysis. In: Borkowsky D (ed) Multivariate data analysis. Prentice-Hall, Englewood Cliffs, NJ, pp 364–404Google Scholar
  12. Holmes G (1917) The symptoms of acute cerebellar injuries due to gunshot injuries. Brain 40:461–535CrossRefGoogle Scholar
  13. Horak FB, Diener HC (1994) Cerebellar control of postural scaling and central set in stance. J Neurophysiol 72:479–493PubMedGoogle Scholar
  14. Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556:267–282PubMedCrossRefGoogle Scholar
  15. Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F (2005) Coordination of locomotion with voluntary movements in humans. J Neurosci 25:7238–7253PubMedCrossRefGoogle Scholar
  16. Krishnamoorthy V, Goodman S, Zatsiorsky VM, Latash ML (2003a) Muscle synergies during shifts of the center of pressure by standing persons: identification of muscle modes. Biol Cybern 89:152–161PubMedCrossRefGoogle Scholar
  17. Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003b) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292PubMedCrossRefGoogle Scholar
  18. 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 157:18–31PubMedCrossRefGoogle Scholar
  19. Küng UM, Horlings CGC, Honegger F, Kremer HPH, Bloem BR, van de Warrenburg BP, Allum JH (2009) Postural instability in cerebellar ataxia: correlations of knee, arm and trunk movements to center of mass velocity. Neuroscience 159:390–404PubMedCrossRefGoogle Scholar
  20. Latash ML, Scholz JP, Schöner G (2002) Motor control strategies revealed in the structure of motor variability. Exer Sport Sci Rev 30:26–31CrossRefGoogle Scholar
  21. Masani K, Vette AH, Popovic MR (2006) Controlling balance during quiet standing: proportional and derivative controller generates preceding motor command to body sway position observed in experiments. Gait Posture 23:164–172PubMedCrossRefGoogle Scholar
  22. Massion J (1992) Movement, posture and equilibrium interaction and coordination. Prog Neurobiol 38:35–56PubMedCrossRefGoogle Scholar
  23. Olafsdottir HB, Kim SW, Zatsiorsky VM, Latash ML (2008) Anticipatory synergy adjustments in preparation to self-triggered perturbations in elderly individuals. J Appl Biomech 24:175–179PubMedGoogle Scholar
  24. Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118PubMedGoogle Scholar
  25. Robert T, Latash ML (2008) Time evolution of the organization of multi-muscle postural responses to sudden changes in the external force applied at the trunk level. Neurosci Lett 438:238–241PubMedCrossRefGoogle Scholar
  26. Schepens B, Drew T (2004) Independent and convergent signals from the pontomedullary reticular formation contribute to the control of posture and movement during reaching in the cat. J Neurophysiol 94:2217–2238CrossRefGoogle Scholar
  27. Schepens B, Drew T (2006) Descending signals from the pontomedullary reticular formation are bilateral, asymmetric and gated during reaching movements in the cat. J Neurophysiol 96:2229–2252PubMedCrossRefGoogle Scholar
  28. Schepens B, Stapley PJ, Drew T (2008) Neurones in the pontomedullary reticular formation signal posture and movement both as an integrated behavior and independently. J Neurophysiol 100:2235–2254PubMedCrossRefGoogle Scholar
  29. Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306PubMedCrossRefGoogle Scholar
  30. Timmann D, Horak FB (1997) Prediction and set-dependent scaling of early posture responses in cerebellar patients. Brain 120:327–337PubMedCrossRefGoogle Scholar
  31. Timmann D, Horak FB (2001) Perturbed step initiation in cerebellar subjects: 2. Modification of anticipatory postural adjustments. Exp Brain Res 141:110–120PubMedCrossRefGoogle Scholar
  32. Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609–613PubMedCrossRefGoogle Scholar
  33. Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5:1226–1235PubMedCrossRefGoogle Scholar
  34. Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramony SH, Wessel K, Bryer A, Diener HC, Massaquoi S, Gomez CM, Coutinho P, Ben Hamida M, Campanella G, Filla A, Schut L, Timann D, Honnorat J, Nighoghossian N, Manyam B (1997) International cooperative ataxia rating scale for pharmacological assessment of the cerebellar syndrome. The ataxia neuropharmacology committee of the world federation of neurology. J Neurol Sci 145:205–211PubMedCrossRefGoogle Scholar
  35. Wang Y, Asaka T (2008) Muscle synergies involved in shifts of the center of pressure while standing on a narrow support. Brain Res Bull 76:16–25PubMedCrossRefGoogle Scholar
  36. Wang Y, Zatsiorsky VM, Latash ML (2005) Muscle synergies involved in shifting the center of pressure while making a first step. Exp Brain Res 167:196–210PubMedCrossRefGoogle Scholar
  37. Wang Y, Asaka T, Zatsiorsky VM, Latash ML (2006) Muscle synergies during voluntary body sway: combining across-trials and within-a-trial analyses. Exp Brain Res 174:679–693PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Rehabilitation Science, Research Faculty of Health SciencesHokkaido UniversityKita-kuJapan
  2. 2.Department of Infant EducationIwakuni Junior CollegeIwakuniJapan

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