Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Combinations of muscle synergies in the construction of a natural motor behavior

Nature Neuroscience volume 6, pages 300–308 (2003)Cite this article

Abstract

A central issue in motor control is how the central nervous system generates the muscle activity patterns necessary to achieve a variety of behavioral goals. The many degrees of freedom of the musculoskeletal apparatus provide great flexibility but make the control problem extremely complex. Muscle synergies—coherent activations, in space or time, of a group of muscles—have been proposed as building blocks that could simplify the construction of motor behaviors. To evaluate this hypothesis, we developed a new method to extract invariant spatiotemporal components from the simultaneous recordings of the activity of many muscles. We used this technique to analyze the muscle patterns of intact and unrestrained frogs during kicking, a natural defensive behavior. Here we show that combinations of three time-varying muscle synergies underlie the variety of muscle patterns required to kick in different directions, that the recruitment of these synergies is related to movement kinematics, and that there are similarities among the synergies extracted from different behaviors.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Time-varying synergies model.
Figure 2: Selection of the number of synergies.
Figure 3: Three time-varying synergies extracted from the entire kicking dataset.
Figure 4: Synergies extracted from individual animals.
Figure 5: Reconstruction of kick muscle patterns as combinations of time-varying synergies.
Figure 6: Relationship between kick kinematics and recruitment of two synergies.
Figure 7: Comparison among synergies extracted from kicking, jumping, swimming and walking.

Similar content being viewed by others

References

  1. Bernstein, N. The Co-ordination and Regulation of Movement (Pergamon, Oxford, 1967).

    Google Scholar 

  2. Hogan, N. Planning and execution of multijoint movements. Can. J. Physiol. Pharmacol. 66, 508–517 (1988).

    Article  CAS  Google Scholar 

  3. Sherrington, C.S. The Integrative Action of the Nervous System (Univeristy Press, Cambridge, England, 1948).

    Google Scholar 

  4. Grillner, S. Control of locomotion in bipeds, tetrapods and fish. in Handbook of Physiology: Sect I. The Nervous System (ed. Brooks, V.B.) 1179–1236 (American Physiological Society, Bethesda, Maryland, 1981).

    Google Scholar 

  5. Bizzi, E., Mussa-Ivaldi, F.A. & Giszter, S.F. Computations underlying the execution of movement: a biological perspective. Science 253, 287–291 (1991).

    Article  CAS  Google Scholar 

  6. Giszter, S.F., Mussa-Ivaldi, F.A. & Bizzi, E. Convergent force fields organized in the frog's spinal cord. J. Neurosci. 13, 467–491 (1993).

    Article  CAS  Google Scholar 

  7. Mussa-Ivaldi, F.A., Giszter, S.F. & Bizzi, E. Linear combinations of primitives in vertebrate motor control. Proc. Natl. Acad. Sci. USA 91, 7534–7538 (1994).

    Article  CAS  Google Scholar 

  8. Tresch, M.C., Saltiel, P. & Bizzi, E. The construction of movement by the spinal cord. Nat. Neurosci. 2, 162–167 (1999).

    Article  CAS  Google Scholar 

  9. Saltiel, P., Wyler-Duda, K., D'Avella, A., Tresch, M.C. & Bizzi, E. Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J. Neurophysiol. 85, 605–619 (2001).

    Article  CAS  Google Scholar 

  10. Lee, W.A. Neuromotor synergies as a basis for coordinated intentional action. J. Mot. Behav. 16, 135–170 (1984).

    Article  CAS  Google Scholar 

  11. Macpherson, J.M. How flexible are muscle synergies? in Motor Control: Concepts and Issues (eds. Humphrey, D.R. & Freund, H.-J.) 33–47 (Wiley, Chichester, UK, 1991).

    Google Scholar 

  12. d'Avella, A. & Tresch, M.C. Modularity in the motor system: decomposition of muscle patterns as combinations of time-varying synergies. in Advances in Neural Information Processing Systems 14 (eds. Dietterich, T.G., Becker, S. & Ghahramani, Z.) 141–148 (MIT Press, Massachusetts, 2002).

    Google Scholar 

  13. Bishop, C. Neural Networks for Pattern Recognition (Claredon, Oxford, UK, 1995).

    Google Scholar 

  14. Mardia, K.V., Kent, J.T. & Bibby, J.M. Multivariate Analysis (Academic, London; New York, 1979).

    Google Scholar 

  15. Bell, A.J. & Sejnowski, T.J. An information-maximization approach to blind separation and blind deconvolution. Neural Comput. 7, 1129–1159 (1995).

    Article  CAS  Google Scholar 

  16. Makeig, S., Jung, T.P., Bell, A.J., Ghahremani, D. & Sejnowski, T.J. Blind separation of auditory event-related brain responses into independent components. Proc. Natl. Acad. Sci. USA 94, 10979–10984 (1997).

    Article  CAS  Google Scholar 

  17. Lee, D.D. & Seung, H.S. Learning the parts of objects by non-negative matrix factorization. Nature 401, 788–791 (1999).

    Article  CAS  Google Scholar 

  18. Sherrington, C.S. Flexion-reflex of the limb, crossed extension reflex and reflex stepping and standing. J. Physiol. (Lond.) 40, 28–121 (1910).

    Article  CAS  Google Scholar 

  19. Brown, T.G. The intrinsic factors in the act of progression in the mammal. Proc. R. Soc. Lond. B Biol. Sci. 84, 308–319 (1911).

    Article  Google Scholar 

  20. Grillner, S. & Zangger, P. On the central generation of locomotion in the low spinal cat. Exp. Brain Res. 34, 241–261 (1979).

    Article  CAS  Google Scholar 

  21. Rossignol, S. & Dubuc, R. Spinal pattern generation. Curr. Opin. Neurobiol. 4, 894–902 (1994).

    Article  CAS  Google Scholar 

  22. Stein, P.S., McCullough, M.L. & Currie, S.N. Spinal motor patterns in the turtle. Ann. NY Acad. Sci. 860, 142–154 (1998).

    Article  CAS  Google Scholar 

  23. Cheng, J. et al. Identification, localization, and modulation of neural networks for walking in the mudpuppy (Necturus maculatus) spinal cord. J. Neurosci. 18, 4295–4304 (1998).

    Article  CAS  Google Scholar 

  24. Saltiel, P., Tresch, M.C. & Bizzi, E. Spinal cord modular organization and rhythm generation: an NMDA iontophoretic study in the frog. J. Neurophysiol. 80, 2323–2339 (1998).

    Article  CAS  Google Scholar 

  25. Kargo, W.J. & Giszter, S.F. Rapid correction of aimed movements by summation of force-field primitives. J. Neurosci. 20, 409–426 (2000).

    Article  CAS  Google Scholar 

  26. Buchanan, T.S., Almdale, D.P.J., Lewis, J.L. & Rymer, W.Z. Characteristics of synergic relations during isometric contractions of human elbow muscles. J. Neurophysiol. 56, 1225–1241 (1986).

    Article  CAS  Google Scholar 

  27. Maier, M.A. & Hepp-Reymond, M.C. EMG activation patterns during force production in precision grip. II. Muscular synergies in the spatial and temporal domain. Exp. Brain Res. 103, 123–136 (1995).

    Article  CAS  Google Scholar 

  28. Soechting, J.F. & Lacquaniti, F. An assessment of the existence of muscle synergies during load perturbations and intentional movements of the human arm. Exp. Brain Res. 74, 535–548 (1989).

    Article  CAS  Google Scholar 

  29. Macpherson, J.M. Strategies that simplify the control of quadrupedal stance. II. Electromyographic activity. J. Neurophysiol. 60, 218–231 (1988).

    Article  CAS  Google Scholar 

  30. Henry, S.M., Fung, J. & Horak, F.B. EMG responses to maintain stance during multidirectional surface translations. J. Neurophysiol. 80, 1939–1950 (1998).

    Article  CAS  Google Scholar 

  31. Wadman, W., Dernier van der Gon, J.J. & Derksen, R.J.A. Muscle activation patterns for fast goal-directed arm movements. J. Hum. Mov. Stud. 6, 19–37 (1980).

    Google Scholar 

  32. Karst, G.M. & Hasan, Z. Timing and magnitude of electromyographic activity for two-joint arm movements in different directions. J. Neurophysiol. 66, 1594–1604 (1991).

    Article  CAS  Google Scholar 

  33. Flanders, M., Pellegrini, J.J. & Soechting, J.F. Spatial/temporal characteristics of a motor pattern for reaching. J. Neurophysiol. 71, 811–813 (1994).

    Article  CAS  Google Scholar 

  34. Hoffman, D.S. & Strick, P.L. Step-tracking movements of the wrist. IV. Muscle activity associated with movements in different directions. J. Neurophysiol. 81, 319–333 (1999).

    Article  CAS  Google Scholar 

  35. Scott, S.H. Comparison of onset time and magnitude of activity for proximal arm muscles and motor cortical cells before reaching movements. J. Neurophysiol. 77, 1016–1022 (1997).

    Article  CAS  Google Scholar 

  36. Ecker, A. The Anatomy of the Frog (Claredon, Oxford, 1889).

    Google Scholar 

  37. Lombard, W.P. & Abbott, F.M. The mechanical effect produced by the contraction of individual muscles of the thigh of the frog. Am. J. Physiol. 20, 1–60 (1907).

    Article  Google Scholar 

  38. Kargo, W.J. & Rome, L.C. Functional morphology of proximal hindlimb muscles in the frog Rana pipiens. J. Exp. Biol. 205, 1987–2004 (2002).

    PubMed  Google Scholar 

  39. Lee, D.D. & Seung, H.S. Algorithms for non-negative matrix factorization. in Advances in Neural Information Processing Systems Vol. 13 (eds. Leen, T.K., Dietterich, T.G. & Tresp, V.) 556–562 (MIT Press, Massachusetts, 2001).

    Google Scholar 

Download references

Acknowledgements

We thank M. Tresch for many helpful discussions and suggestions, S. Mussa-Ivaldi, M. Mezzetti, D. Grodner, A. Rebek and C. Gulledge for comments on the manuscript, S. Dalai and J. O'Vari for helping with the experiments and the analysis of kinematic data, and M. Cantor for constant and irreplaceable support. Supported by NIH-NINDS NS09343.

Author information

Authors and Affiliations

  1. Department of Brain and Cognitive Sciences and McGovern Institute for Brain Research, Massachusetts Institute of Technology, 45 Carleton St., Cambridge, 02139, Massachusetts, USA

    Andrea d'Avella, Philippe Saltiel & Emilio Bizzi

  2. Human Physiology Section, IRCCS Fondazione Santa Lucia, Via Ardeatina 306, Rome, 00179, Italy

    Andrea d'Avella

Authors
  1. Andrea d'Avella
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philippe Saltiel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emilio Bizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emilio Bizzi.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

d'Avella, A., Saltiel, P. & Bizzi, E. Combinations of muscle synergies in the construction of a natural motor behavior. Nat Neurosci 6, 300–308 (2003). https://doi.org/10.1038/nn1010

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1010

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing