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.

The construction of movement by the spinal cord

Abstract

We used a computational analysis to identify the basic elements with which the vertebrate spinal cord constructs one complex behavior. This analysis extracted a small set of muscle synergies from the range of muscle activations generated by cutaneous stimulation of the frog hindlimb. The flexible combination of these synergies was able to account for the large number of different motor patterns produced by different animals. These results therefore demonstrate one strategy used by the vertebrate nervous system to produce movement in a computationally simple manner.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Muscle activation patterns evoked from cutaneous stimulation of the frog hindlimb.
Figure 2: Example of muscle covariation patterns within evoked responses.
Figure 3: The contribution of each muscle synergy to responses evoked from different regions of the skin surface for three different animals (a, b, c).
Figure 4: The ability of synergies from sites on the rostral and caudal margins of the hindlimb to explain responses evoked from other skin regions.

References

  1. 1

    Bernstein, N. The Coordination and Regulation of Movements (Pergamon Press, New York, 1967).

    Google Scholar 

  2. 2

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

    CAS  Article  Google Scholar 

  3. 3

    Macpherson, J. M. in Motor Control: Concepts and Issues (eds. Humphrey, D. R. & Freund, H.–J) 33–47 (Wiley, Chichester, 1991).

    Google Scholar 

  4. 4

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

    CAS  Article  Google Scholar 

  5. 5

    Grillner, S. in Handbook of Physiology, sec. 1, vol. 2 (ed. Brooks, V. B.) 1179 –1236 (American Physiological Society, Bethesda, MD, 1981).

    Google Scholar 

  6. 6

    Stein, P. S. G. & Smith J. L. in Neurons, Networks, and Motor Behavior (eds. Stein P. S. G., Grillner, S., Selverston A. I. & Stuart D. G.) 61–73 (MIT Press, Cambridge, MA, 1997).

    Google Scholar 

  7. 7

    Jacobs, R. & Macpherson, J. M. Two functional muscle groupings during postural equilibrium tasks in standing cats. J. Neurophysiol. 76, 2402–2411 ( 1996).

    CAS  Article  Google Scholar 

  8. 8

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

    CAS  Article  Google Scholar 

  9. 9

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

    CAS  Article  Google Scholar 

  10. 10

    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  Google Scholar 

  11. 11

    Bishop, C. M. Neural Networks for Pattern Recognition (Oxford Univ. Press, Oxford, 1995).

    Google Scholar 

  12. 12

    Hertz, J., Krogh, A. & Palmer R. G. Introduction to the Theory of Neural Computation (Addison–Wesley, Reading, MA 1991).

    Google Scholar 

  13. 13

    d'Avella, A. & Bizzi, E. Low dimensionality of supraspinally induced force fields. Proc. Natl. Acad. Sci. USA 95, 7711–7714 (1998).

    CAS  Article  Google Scholar 

  14. 14

    Fleshman, J. W., Lev–Tov, A. & Burke, R. E. Peripheral and central control of flexor digitorum longus and flexor hallucis longus motoneurons: the synaptic basis of functional diversity. Exp. Brain Res. 54, 133– 149 (1984).

    CAS  Article  Google Scholar 

  15. 15

    Pratt, C. A., Chanaud, C. M. & Loeb, G. E. Functionally complex muscles of the cat hindlimb. IV. Intramuscular distribution of movement command signals and cutaneous reflexes in broad, bifunctional thigh muscles. Exp. Brain Res. 85, 281–299 (1991).

    CAS  Article  Google Scholar 

  16. 16

    Schouenborg, J. & Kalliomaki, J. Functional organization of the nociceptive withdrawal reflexes I. Activation of hindlimb muscles in the rat. Exp. Brain Res. 83, 67–78 (1990).

    CAS  Article  Google Scholar 

  17. 17

    Schouenborg, J. & Weng, H.–R. Sensorimotor transformations in a spinal motor system. Exp. Brain Res. 100, 170–174 (1994).

    CAS  Article  Google Scholar 

  18. 18

    Schouenborg, J., Weng, H.–R. & Holmberg, H. Modular organization of spinal nociceptive reflexes: a new hypothesis. News Physiol. Sci. 9, 261–265 (1994).

    Google Scholar 

  19. 19

    Berkinblitt, M. B., Feldman, A. G. & Fukson, O. I. Adaptability of innate motor patterns and motor control mechanisms. Behav. Brain Sci. 9, 585– 638 (1986).

    Article  Google Scholar 

  20. 20

    Lawson, C. L. & Hanson, R. J. Solving Least Squares Problems. (Prentice–Hall, Englewood Cliffs, NJ, 1974).

    Google Scholar 

  21. 21

    Harman, H. H. Modern Factor Analysis (Univ. of Chicago Press, Chicago, 1976).

    Google Scholar 

  22. 22

    Olshausen, B. A. & Field, D. J. Emergence of simple–cell receptive field properties by learning a sparse code for natural images. Nature 381, 607– 609 (1996).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank Sandro Mussa–Ivaldi and Andrea d'Avella for reading versions of this manuscript and Simon Giszter, Peter Dayan, Kuno Wyler and James Galagan for suggestions. M.C.T. was supported by a HHMI predoctoral fellowship. This research was supported by NIH NS09343 and ONR N00014–95–I0445 to E.B.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Emilio Bizzi.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tresch, M., Saltiel, P. & Bizzi, E. The construction of movement by the spinal cord. Nat Neurosci 2, 162–167 (1999). https://doi.org/10.1038/5721

Download citation

Further reading

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