Skip to main content

Advertisement

Log in

Multi-muscle synergies in a dual postural task: evidence for the principle of superposition

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

We used the framework of the uncontrolled manifold hypothesis to quantify multi-muscle synergies stabilizing the moment of force about the frontal axis (M Y) and the shear force in the anterior–posterior direction (F X) during voluntary body sway performed by standing subjects. We tested a hypothesis whether the controller could stabilize both M Y and F X at the same time when the task and the visual feedback was provided only on one of the variables (M Y). Healthy young subjects performed voluntary body sway in the anterior–posterior direction while different loads were attached at the ankle level producing horizontal forces acting forward or backwards. Principal component analysis was used to identify three M-modes within the space of integrated indices of muscle activation. Variance in the M-mode space across sway cycles was partitioned into two components, one that did not affect a selected performance variable (M Y or F X) and the other that did. Under all loading conditions and for each performance variable, a higher value for the former variance component was found. We interpret these results as reflections of two multi-M-mode synergies stabilizing both F X and M Y. The indices of synergies were modulated within the sway cycle; both performance variables were better stabilized when the body moved forward than when it moved backward. The results show that the controller can use a set of three elemental variables (M-modes) to stabilize two performance variables at the same time. No negative interference was seen between the synergy indices computed for the two performance variables supporting the principle of superposition with respect to multi-muscle postural control.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Arimoto S, Tahara K, Yamaguchi M, Nguyen PTA, Han H-Y (2001) Principles of superposition for controlling pinch motions by means of robot fingers with soft tips. Robotica 19:21–28

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bernstein NA (1935) The problem of interrelation between coordination and localization. Arch Biol Sci 38:1–35 (in Russian)

    Google Scholar 

  • Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon Press, Oxford

    Google Scholar 

  • Bradley NS, Bekoff A (1990) Development of coordinated movements in chicks: I. Temporal analysis of hindlimb muscle synergies at embryonic days 9 and 10. Dev Psychobiol 23:763–782

    Article  CAS  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

    Article  PubMed  Google Scholar 

  • Danna-dos-Santos A, Slomka K, Latash ML, Zatsiorsky VM (2007) Muscle modes and synergies during voluntary body sway. Exp Brain Res 179:533–550

    Article  PubMed  Google Scholar 

  • Danna-dos-Santos A, Degani AM, Latash ML (2008) Flexible muscle modes and synergies in challenging whole-body tasks. Exp Brain Res 189:171–187

    Article  PubMed  Google Scholar 

  • Demieville HN, Partridge LD (1980) Probability of peripheral interaction between motor units and implications for motor control. Am J Physiol 238:R119–R137

    CAS  PubMed  Google Scholar 

  • Fingelkurts AA, Filngelkurts AA (2006) Stability, reliability and consistency of the compositions of brain oscillations. Int J Psychophysiol 59:116–126

    Article  PubMed  Google Scholar 

  • Friedman J, SKM V, Zatsiorsky VM, Latash ML (2009) The sources of two components of variance: an example of multifinger cyclic force production tasks at different frequencies. Exp Brain Res 196:263–277

    Article  PubMed  Google Scholar 

  • Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Mot Control 2:306–313

    CAS  Google Scholar 

  • Gelfand IM, Tsetlin ML (1966) On mathematical modeling of the mechanisms of the central nervous system. In: Gelfand IM, Gurfinkel VS, Fomin SV, Tsetlin ML (eds) Models of the structural-functional organization of certain biological systems. Nauka, Moscow, pp 9–36 (in Russian, a translation is available in 1971 edition by MIT Press, Cambridge)

  • Gera G, Freitas SMSF, Latash ML, Monahan K, Schöner G, Scholz JP (2009) Motor abundance contributes to resolving multiple kinematic task constraints. Motor Control (in press)

  • Glazer VD, Gauzelman VE (1997) Linear and nonlinear properties of simple cells of the striate cortex of the cat: two types of nonlinearity. Exp Brain Res 117:281291

    Google Scholar 

  • Goodman SR, Shim JK, Zatsiorsky VM, Latash ML (2005) Motor variability within a multi-effector system: experimental and analytical studies of multi-finger production of quick force pulses. Exp Brain Res 163:75–85

    Article  PubMed  Google Scholar 

  • Gorniak SL, Duarte M, Latash ML (2008) Do synergies improve accuracy? A study of speed-accuracy trade-offs during finger force production. Motor Control 12:151–172

    PubMed  Google Scholar 

  • Gorniak SL, Zatsiorsky VM, Latash ML (2009) Hierarchical control of static prehension: II. Multi-digit synergies. Exp Brain Res 194:1–15

    Article  PubMed  Google Scholar 

  • Hair JF, Anderson RE, Tatham RL, Black WC (1995) Factor analysis. In: Borkowsky D (ed) Multivariate data analysis. Prentice-Hall, Englewood Cliffs, pp 364–404

    Google Scholar 

  • Henry SM, Fung J, Horak FB (1998) EMG responses to maintain stance during multidirectional surface translation. J Neurophysiol 80:1939–1950

    CAS  PubMed  Google Scholar 

  • Hogan N, Sternad D (2007) On rhythmic and discrete movements: reflections, definitions and implications for motor control. Exp Brain Res 181:13–30

    Article  PubMed  Google Scholar 

  • Holdefer RN, Miller LE (2002) Primary motor cortical neurons encode functional muscle synergies. Exp Brain Res 146:233–243

    Article  CAS  PubMed  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Ivanenko YP, Wright WG, Gurfinkel VS, Horak F, Cordo P (2006) Interaction of involuntary post-contraction activity with locomotor movements. Exp Brain Res 169:255–260

    Article  CAS  PubMed  Google Scholar 

  • Johnson RM, Bekoff A (1996) Patterns of muscle activity during different behaviors in chicks: implications for neural control. J Comp Physiol 179:169–184

    Google Scholar 

  • Karakas S, Erzengin OU, Basar E (2000) A new strategy involving multiple cognitive paradigms demonstrates that ERP components are determined by the superposition of oscillatory responses. Clin Neurophysiol 111:1719–1732

    Article  CAS  PubMed  Google Scholar 

  • Kowalski N, Depireux DA, Shamma SA (1996) Analysis of dynamic spectra in ferret primary auditory cortex. II Prediction of unit responses to arbitrary dynamic spectra. J Neurophysiol 76:3524–3534

    CAS  PubMed  Google Scholar 

  • Krishnamoorthy V, Latash ML (2005) Reversals of anticipatory postural adjustments during voluntary sway in humans. J Physiol 565:675–684

    Article  CAS  PubMed  Google Scholar 

  • Krishnamoorthy V, Goodman SR, Latash ML, Zatsiorsky VM (2003a) Muscle synergies during shifts of the center of pressure by standing persons: identification of muscle modes. Biol Cybern 89:152–161

    Article  PubMed  Google Scholar 

  • Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003b) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Latash ML (2008) Synergy. Oxford University Press, New York

    Book  Google Scholar 

  • Latash ML, Scholz JF, Danion F, Schöner G (2002a) Finger coordination during discrete and oscillatory force production tasks. Exp Brain Res 146:412–432

    Google Scholar 

  • Latash ML, Scholz JP, Schöner G (2002b) Motor control strategies revealed in the structure of motor variability. Exerc Sport Sci Rev 30:26–31

    Article  PubMed  Google Scholar 

  • Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Motor Control 11:275–307

    Google Scholar 

  • Latt LD, Sparto PJ, Fruman JM, Redfern MS (2003) The steady-state postural response to continuous sinusoidal galvanic vestibular stimulation. Gait Posture 18:64–72

    Article  CAS  PubMed  Google Scholar 

  • Lemay MA, Grill WM (2004) Modularity of motor output evoked by intraspinal microstimulation in cats. J Neurophysiol 91:502–514

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Ruegg DG, Bongioanni F (1989) Superposition of ballistic on steady contractions in man. Exp Brain Res 77:412–420

    Article  CAS  PubMed  Google Scholar 

  • Saltiel P, Wyler-Duda K, d’Avella A, Tresch MC, Bizzi E (2001) Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J Neurophysiol 5:605–619

    Google Scholar 

  • Schaal S, Sternad D, Osu R, Kawato M (2004) Rhythmic arm movement is not discrete. Nat Neurosci 7:1136–1143

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Shapkova EY, Shapkova AL, Goodman SR, Zatsiorsky VM, Latash ML (2008) Do synergies decrease force variability? A study of single-finger and multi-finger force production. Exp Brain Res 188:411–425

    Article  PubMed  Google Scholar 

  • Shim JK, Park J (2007) Prehension synergies: principle of superposition and hierarchical organization in circular object prehension. Exp Brain Res 180:541–556

    Article  PubMed  Google Scholar 

  • Shim JK, Latash ML, Zatsiorsky VM (2003) Prehension synergies: trial-to-trial variability and hierarchical organization of stable performance. Exp Brain Res 152:173–178

    Article  PubMed  Google Scholar 

  • Shim JK, Latash ML, Zatsiorsky VM (2005a) Prehension synergies: trial-to-trial variability and principle of superposition during static prehension in three dimensions. J Neurophysiol 93:3649–3658

    Article  PubMed  Google Scholar 

  • Shim JK, Olafsdottir H, Zatsiorsky VM, Latash ML (2005b) The emergence and disappearance of multi-digit synergies during force production tasks. Exp Brain Res 164:260–270

    Article  PubMed  Google Scholar 

  • Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609–613

    Article  PubMed  Google Scholar 

  • Ting LH, McKay JL (2007) Neuromechanics of muscle synergies for posture and movement. Curr Opin Neurobiol 17:622–628

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Tresch MC, Cheung VC, d’Avella A (2006) Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. J Neurophysiol 95:2199–2212

    Article  PubMed  Google Scholar 

  • Turvey MT (1990) Coordination. Am Psychol 45:938–953

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wang Y, Zatsiorsky VM, Latash ML (2006) 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 

  • Weiss EJ, Flanders M (2004) Muscular and postural synergies of the human hand. J Neurophysiol 92:523–535

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM, Latash ML, Gao F, Shim JK (2004) The principle of superposition in human prehension. Robotica 22:231–234

    Article  PubMed  Google Scholar 

  • Zhang W, Scholz JP, Zatsiorsky VM, Latash ML (2008) What do synergies do? Effects of secondary constraints on multidigit synergies in accurate force-production tasks. J Neurophysiol 99:500–513

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The study was in part supported by NIH grants NS-035032 and AG-018751. We are grateful to Elena Shapkova and Jason Friedman for their help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark L. Latash.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Klous, M., Danna-dos-Santos, A. & Latash, M.L. Multi-muscle synergies in a dual postural task: evidence for the principle of superposition. Exp Brain Res 202, 457–471 (2010). https://doi.org/10.1007/s00221-009-2153-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-009-2153-2

Keywords

Navigation