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Coupled nonlinear oscillators and the symmetries of animal gaits

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Summary

Animal locomotion typically employs several distinct periodic patterns of leg movements, known as gaits. It has long been observed that most gaits possess a degree of symmetry. Our aim is to draw attention to some remarkable parallels between the generalities of coupled nonlinear oscillators and the observed symmetries of gaits, and to describe how this observation might impose constraints on the general structure of the neural circuits, i.e. central pattern generators, that control locomotion. We compare the symmetries of gaits with the symmetry-breaking oscillation patterns that should be expected in various networks of symmetrically coupled nonlinear oscillators. We discuss the possibility that transitions between gaits may be modeled as symmetry-breaking bifurcations of such oscillator networks. The emphasis is on general model-independent features of such networks, rather than on specific models. Each type of network generates a characteristic set of gait symmetries, so our results may be interpreted as an analysis of the general structure required of a central pattern generator in order to produce the types of gait observed in the natural world. The approach leads to natural hierarchies of gaits, ordered by symmetry, and to natural sequences of gait bifurcations. We briefly discuss how the ideas could be extended to hexapodal gaits.

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References

  • Alexander, J.C. (1986). Patterns at primary Hopf bifurcations of a plexus of identical oscillators.SIAM J. Appl. Math. 46, 199–221.

    Article  MATH  MathSciNet  Google Scholar 

  • Alexander, R. McN. (1984). The gaits of bipedal and quadrupedal animals.Int. J. Robot. Res. 3(2), 49–59.

    MathSciNet  Google Scholar 

  • Alexander, R. McN. (1989). Optimization of gaits in the locomotion of vertebrates.Physiol. Rev. 69, 1199–1227.

    MathSciNet  Google Scholar 

  • Aristotle. De Partibus Animalium, De Incessu Animalium, De Motu Animalium. InParts of Animals, Movement of Animals, Progression of Animals (Peek, A.S., and Forster, E.S., translators). Cambridge, MA: Harvard University Press, 1936.

    Google Scholar 

  • Ashwin, P. (1990). Symmetric chaos in systems of three and four forced oscillators.Nonlinearity 3, 603–617.

    Article  MATH  MathSciNet  Google Scholar 

  • Ashwin, P., King, G.P., and Swift, J.W. (1990). Three identical oscillators with symmetric coupling.Nonlinearity 3, 585–601.

    Article  MATH  MathSciNet  Google Scholar 

  • Ashwin, P. and Swift, J.W. (1992). The dynamics ofn weakly coupled identical oscillators.J. Nonlinear Sci. 2, 69–108.

    Article  MATH  MathSciNet  Google Scholar 

  • Baesens, C., Guckenheimer, J., Kim, S., and MacKay, R.S. (1991). Three coupled oscillators: Mode-locking, global bifurcations, and toroidal chaos.Physica D 49, 387–475.

    Article  MATH  MathSciNet  Google Scholar 

  • Bay, J.S. and Hemami, H. (1987). Modeling of a neural pattern generator with coupled nonlinear oscillators.IEEE Trans. Biomed. Eng. 34, 297–306.

    Google Scholar 

  • Brown, T.G. (1911). The intrinsic factors in the act of progression in the mammal.Proc. Roy. Soc. B 84, 308–319.

    Article  Google Scholar 

  • Brown, T.G. (1914). On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system.J. Physiol. (Lond.) 48, 18–46.

    Google Scholar 

  • Calabrese, R.L. (1980). Invertebrate central pattern generators: Modeling and complexity.Behav. Brain Sci. 3, 542–543.

    Google Scholar 

  • Cohen, A.H. (1988). Evolution of the vertebrate central pattern generator for locomotion. InNeural Control of Rhythmic Movements in Vertebrates (Cohen, A.H., Rossignol, S., and Grillner, S., eds.). New York: Wiley, 129–166.

    Google Scholar 

  • Cohen, A.H., Holmes, P.J., and Rand, R.H. (1982). The nature of the coupling between segmental oscillators of the lamprey spinal generator for locomotion: A mathematical model.J. Math. Biol. 13, 345–369.

    Article  MATH  MathSciNet  Google Scholar 

  • Collins, J.J. and Stewart, I.N. (1992). Symmetry-breaking bifurcation: A possible mechansim for 2:1 frequency-locking in animal locomotion.J. Math. Biol. 30, 827–838.

    Article  MATH  MathSciNet  Google Scholar 

  • Collins, J.J. and Stewart, I. (1993). Hexapodal gaits and coupled nonlinear oscillator models.Biol. Cybern 68, 287–298.

    Article  MATH  Google Scholar 

  • Crawford, J.D., Golubitsky, M., Gomes, M.G.M., Knoblach, E., and Stewart, I.N. (1991). Boundary conditions as symmetry constraints. InSingularities, Bifurcations, and Dynamics: Proceedings of Symposium on Singularity Theory and Its Applications, Warwick 1989 (Roberts, M.R. and Stewart, I.N., eds.), vol. 2. Lecture Notes in Mathematics Series, Springer-Verlag, Heidelberg, 63–79.

    Google Scholar 

  • Dagg, A.I. (1973). Gaits in mammals.Mammal Rev. 3(4), 135–154.

    Google Scholar 

  • Davis, J. (1981).Garfield: Bigger than Life. New York: Ballantine.

    Google Scholar 

  • Delcomyn, F. (1980). Neural basis of rhythmic behavior in animals.Science 210, 492–498.

    Google Scholar 

  • Epstein, I. and Golubitsky, M. (1992). Linear arrays of coupled cells. Preprint, University of Houston.

    Google Scholar 

  • Ermentrout, G.B. (1986). The behavior of rings of coupled oscillators.J. Math. Biol. 23, 55–74.

    MathSciNet  Google Scholar 

  • Gaeta, G. (1990). Bifurcation and symmetry breaking.Phys. Reports 189, 1–87.

    Article  MathSciNet  Google Scholar 

  • Gambaryan, P. (1974).How Mammals Run: Anatomical Adaptations. New York: Wiley.

    Google Scholar 

  • Glass, L. and Young, R. E. (1979). Structure and dynamics of neural network oscillators.Brain Res. 179, 207–218.

    Article  Google Scholar 

  • Golubitsky, M. and Stewart, I.N. (1985). Hopf bifurcation in the presence of symmetry.Arch. Rational Mech. Anal. 87, 107–165.

    Article  MATH  MathSciNet  Google Scholar 

  • Golubitsky, M. and Stewart, I.N. (1986). Hopf bifurcation with dihedral group symmetry: Coupled nonlinear oscillators. InMultiparameter Bifurcation Theory (Golubitsky, M. and Guckenheimer, J., eds.). Contemporary Math.56, Amer. Math. Soc., Providence, 131–173.

    Google Scholar 

  • Golubitsky, M., Stewart, I.N., and Schaeffer, D.G. (1988).Singularities and Groups in Bifurcation Theory, vol. II. New York: Springer.

    Google Scholar 

  • Grasman, J. and Jansen, M.J.W. (1979). Mutually synchronized relaxation oscillators as prototypes of oscillating systems in biology.J. Math. Biol. 7, 171–197.

    MATH  MathSciNet  Google Scholar 

  • Gray, J. (1968).Animal Locomotion. London: Weidenfeld and Nicolson.

    Google Scholar 

  • Grillner, S. (1975). Locomotion in vertebrates: Central mechanisms and reflex interaction.Physiol. Rev. 55, 247–304.

    Article  Google Scholar 

  • Grillner, S. (1985). Neurobiological bases for rhythmic motor acts in vertebrates.Science 228, 143–149.

    Google Scholar 

  • Grillner, S. and Wallén, P. (1985). Central pattern generators for locomotion, with special reference to vertebrates.Ann. Rev. Neurosci. 8, 233–261.

    Article  Google Scholar 

  • Guckenheimer, J. and Kim, S. (1990).kaos. Mathematical Sciences Institute Technical Report, Cornell University, Ithaca, New York.

    Google Scholar 

  • Herman, R.M., Grillner, S., Stein, P.S.G., and Stuart, D.G., eds. (1976).Neural Control of Locomotion. New York: Plenum Press.

    Google Scholar 

  • Hildebrand, H. (1965). Symmetrical gaits of horses.Science 150, 701–708.

    Google Scholar 

  • Hildebrand, H. (1966). Analysis of the symmetrical gaits of tetrapods.Folia Biotheoretica 4, 9–22.

    Google Scholar 

  • Hildebrand, M. (1968). Symmetircal gaits of dogs in relation to body build.J. Morphol. 124, 353–359.

    Article  Google Scholar 

  • von Holst, E. (1935). Erregungsbildung und Erregungsleitung im Fischrückenmark.Pflügers Arch. 235, 345–359.

    Article  Google Scholar 

  • von Holst, E. (1973).The Behavioral Physiology of Animals and Man. Coral Gables, FL: University of Miami Press.

    Google Scholar 

  • Hoyt, D.F. and Taylor, R.C. (1981). Gait and the energetics of locomotion in horses.Nature 292, 239–240.

    Article  Google Scholar 

  • Kelso, J.A.S. and Schöner, G. (1988). Self-organization of coordinative movement patterns.Human Movement Science 7, 27–46.

    Article  Google Scholar 

  • Kopell, N. (1988). Toward a theory of modelling central pattern generators. InNeural Control of Rhythmic Movements in Vertebrates (Cohen, A.H., Rossignol, S., and Grillner, S., eds.). New York: Wiley, 369–413.

    Google Scholar 

  • Kupfermann, I. and Weiss, K.R. (1978). The command neuron concept.Behav. Brain Sci. 1, 3–39.

    Article  Google Scholar 

  • McGhee, R.B. (1968). Some finite state aspects of legged locomotion.Math. Biosci. 2, 67–84.

    Article  MATH  Google Scholar 

  • McGhee, R.B. and Jain, A.K. (1972). Some properties of regularly realizable gait matrices.Math. Biosci. 13, 179–193.

    Article  MATH  MathSciNet  Google Scholar 

  • Murray, J.D. (1989)Mathematical Biology. Biomathematics Texts 19. New York: Springer-Verlag.

    MATH  Google Scholar 

  • Muybridge, E. (1899).Animals in Motion. London: Chapman and Hall. Republished Dover Publications, New York, 1957.

    Google Scholar 

  • Muybridge, E. (1901).The Human Figure in Motion. London: Chapman and Hall. Republished Dover Publications, New York, 1955.

    Google Scholar 

  • Raibert, M.H. (1986). Running with symmetry.Int. J. Robot. Res. 5, 3–19.

    Google Scholar 

  • Raibert, M.H. (1988). Balance and symmetry in running. InNatural Computation (Richards, W., ed.). Cambridge, MA: MIT Press, 487–503.

    Google Scholar 

  • Rand, R., Cohen, A.H., and Holmes, P.J. (1988). Systems of coupled oscillators as models of central pattern generators. InNeural Control of Rhythmic Movements in Vertebrates (Cohen, A.H., Rossignol, S., and Grillner, S., eds.). New York: Wiley, 333–367.

    Google Scholar 

  • Schmidt-Nielsen, K. (1990).Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press.

    Google Scholar 

  • Schönder, G., Yiang, W. Y., and Kelso, J.A.S. (1990). A synergetic theory of quadrupedal gaits and gait transitions.J. Theor. Biol. 142, 359–391.

    Article  Google Scholar 

  • Selverston, A.I. (1980). Are central pattern generators understandable?Behav. Brain Sci. 3, 535–571.

    Google Scholar 

  • Shik, M.L. and Orlovsky, G.N. (1976). Neurophysiology of locomotor automatism.Physiol. Rev. 56, 465–501.

    Google Scholar 

  • Smale, S. (1974). A mathematical model of two cells via Turing's equation. InSome Mathematical Questions in Biology V (Cowan, J.D., ed.). Amer. Math. Soc. Lecture Notes on Mathematics in the Life Sciences6, Providence, 15–26.

    MathSciNet  Google Scholar 

  • Stein, P.S.G. (1978). Motor systems, with specific reference to the control of locomotion.Ann. Rev. Neurosci. 1, 61–81.

    Article  Google Scholar 

  • Swift, J.W. (1988). Hopf bifurcation with the symmetry of the square.Nonlinearity 1, 333–377.

    Article  MATH  MathSciNet  Google Scholar 

  • Taft, R. (1955). An introduction: Eadweard Muybridge and his work. In Muybridge, E.The Human Figure in Motion. New York: Dover Publications, vii-xiv.

    Google Scholar 

  • Willis, J.B. (1980). On the interaction between spinal locomotor generators in quadrupeds.Brain Res. Rev. 2, 171–204.

    Article  MathSciNet  Google Scholar 

  • Yuasa, H. and Ito, M. (1990). Coordination of many oscillators and generation of locomotory patterns.Biol. Cybern. 63, 177–184.

    Article  MATH  Google Scholar 

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Communicated by James Murray

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Collins, J.J., Stewart, I.N. Coupled nonlinear oscillators and the symmetries of animal gaits. J Nonlinear Sci 3, 349–392 (1993). https://doi.org/10.1007/BF02429870

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