, Volume 3, Issue 3, pp 171–195 | Cite as

Simulation and robotics studies of salamander locomotion

Applying neurobiological principles to the control of locomotion in robots
  • Auke Jan IjspeertEmail author
  • Alessandro Crespi
  • Jean-Marie Cabelguen
Original Article


This article presents a project that aims at understanding the neural circuitry controlling salamander locomotion, and developing an amphibious salamander-like robot capable of replicating its bimodal locomotion, namely swimming and terrestrial walking. The controllers of the robot are central pattern generator models inspired by the salamander’s locomotion control network. The goal of the project is twofold: (1) to use robots as tools for gaining a better understanding of locomotion control in vertebrates and (2) to develop new robot and control technologies for developing agile and adaptive outdoor robots. The article has four parts. We first describe the motivations behind the project. We then present neuromechanical simulation studies of locomotion control in salamanders. This is followed by a description of the current stage of the robotic developments. We conclude the article with a discussion on the usefulness of robots in neuroscience research with a special focus on locomotion control.

Index Entries

Salamander lamprey locomotion gait transition swimming walking, simulation robotics 


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  1. Ashley-Ross, M. (1994a) Hindlimb kinematics during terrestrial locomotion in a salamander (dicampton tenebrosus). J. Exp. Biol. 193,255–283.PubMedGoogle Scholar
  2. Ashley-Ross, M. (1994b) Metamorphic and speed effects on hindlimb kinematics during terrestrial locomotion in the salamander (dicampton tenebrosus). J. Exp. Biol. 193, 285–305.PubMedGoogle Scholar
  3. Ashley-Ross, M. and Bechtel, B. (2004) Kinematics of the transition between aquatic and terrestrial locomotion in the newt Taricha torosa. J. Exp. Biol. 207, 461–474.PubMedCrossRefGoogle Scholar
  4. Ashley-Ross, M. and Lauder, G. (1997) Motor patterns and kinematics during backward walking in the pacific giant salamander: evidence for novel motor output. J. Neurophys. 78, 3047–3060.Google Scholar
  5. Ayers, J. and Crisman, J. (1993) The lobster as a model for an omnidirectional robotic ambulation control architecture. In: Biological Neural Networks in Invertebrate Neuroethology and Robotics. Beer, R., Ritzmann, R., and McKenna, T. (eds.) Academic Press, New York, pp. 287–316.Google Scholar
  6. Bem, T., Cabelguen, J.-M., Ekeberg, O., and Grillner, S. (2003) From swimming to walking: a single basic network for two different behaviors. Biol. Cybern. 88, 79–90.PubMedCrossRefGoogle Scholar
  7. Bowtell, G. and Williams, T. (1991) Anguiliform body dynamics: modelling the interaction between muscle activation and body curvature. Phil. Trans. R. Soc. Lond. B. 334, 385–390.CrossRefGoogle Scholar
  8. Breithaupt, R., Dahnke, J., Zahedi, K., Hertzberg, J., and Pasemann, F. (2002) Robo-salamander—an approach for the benefit of both robotics and biology. In: Clawar (2002).Google Scholar
  9. Buchanan, J. (1992) Neural network simulations of coupled locomotor oscillators in the lamprey spinal cord. Biol. Cybern. 66, 367–374.PubMedCrossRefGoogle Scholar
  10. Buchanan, J. and Grillner, S. (1987) Newly identified ‘glutamate interneurons’ and their role in locomotion in the lamprey spinal cord. Science 236, 312–314.PubMedCrossRefGoogle Scholar
  11. Cabelguen, J. M., Bourcier-Lucas, C., and Dubuc, R. (2003) Bimodal locomotion elicited by electrical stimulation of the midbrain in the salamander notophthalmus viridesecens. J. Neurosci. 23(6), 2434–2439.PubMedGoogle Scholar
  12. Carling, J., Williams, T., and Bowtell, G. (1998) Self-propelled anguiliform swimming: simultaneous solution of the two dimensional Navier-Stokes equations and Newton’s laws of motion. J. Exp. Biol. 201, 3143–3166.PubMedGoogle Scholar
  13. Carrier, D. (1993) Action of the hypaxial muscles during walking and swimming in the salamander dicamptodon ensatus. J. Exp. Biol. 180, 75–63.Google Scholar
  14. Cheng, J., Stein, R., Jovanovic, K., Yoshida, K., Bennett, D., and Han, Y. (1998) Identification, localization, and modulation of neural networks for walking in the mudpuppy (necturus maculatus) spinal cord. J. Neurosci. 18(11), 4295–4304.PubMedGoogle Scholar
  15. Cohen, A. (1988) Evolution of the vertebrate central pattern generator for locomotion. In Neural Control of Rhythmic Movements in Vertebrates. Cohen, A. H., Rossignol, S., and Grillner, S. (eds.) John Wiley & Sons, New York.Google Scholar
  16. Cohen, A. and Wallen, P. (1980) The neural correlate of locomotion in fish. “fictive swimming” induced in an in vitro preparation of the lamprey spinal cord. Exp. Brain Res. 41, 11–18.PubMedCrossRefGoogle Scholar
  17. Collins, J. and Richmond. (1994) Hard-wired central pattern generators for quadrupedal locomotion. Biol. Cybern. 71, 375–385.CrossRefGoogle Scholar
  18. Crepsi, A., Badertscher, A., Guignard, A., and Ijspeert, A. (2005a) Swimming and crawling with an amphibious snake robot. In: IEEE International Conference on Robotics and Automation (ICRA2005) 50(4), 3035–3039.Google Scholar
  19. Crespi, A., Badertscher, A., Guignard, A., and Ijspeert, A. (2005b) AmphiBot I: an amphibious snake-like robot. Robot. Auton. Syst. (In press)Google Scholar
  20. Deliagina, T., Zelenin, P., Fagerstedt, P., Grillner, S., and Orlovsky, G. (2000) Activity of the reticulospinal neurons during locomotion in freely behaving lamprey. J. Neurophys. 83, 853–863.Google Scholar
  21. Delvolvé, I., Bem, T., and Cabelguen, J.-M. (1997) Epaxial and limb muscle activity during swimming and terrestrial stepping in the adult newt, Pleurodeles Waltl. J. Neurophys. 78, 638–650.Google Scholar
  22. Delvolvé, I., Branchereau, P., Dubuc, R., and Cabelguen, J.-M. (1999) Fictive rhythmic motor patterns induced by NMDA in an in vitro brain stem-spinal cord preparation from an adult urodele. J. Neurophys. 82, 1074–1077.Google Scholar
  23. Edwards, J. (1976) The evolution of terrestriallocomotion. In: Major Patterns in Vertebrate Evolution. Hecht, M. K., Goody, P. C, and Hecht, B. M. (eds.) Plenum Press, New York, pp. 553–577.Google Scholar
  24. Ekeberg, O. (1993) A combined neuronal and mechanical model of fish swimming. Biol. Cybern. 69, 363–374.Google Scholar
  25. Ekeberg, O., Wallén, P., Lansner, A., Traven, H., Brodin, L., and Grillner, S. (1991) A computer-based model for realistic simulations of neural networks 1: The single neuron and synaptic interaction. Biol. Cybern. 65, 81–90.PubMedCrossRefGoogle Scholar
  26. Ermentrout, B. and Kopell, N. (1994) Inhibition-produced patterning in chains of coupled nonlinear oscillators. SIAM J. Appl. Math. 54(2), 478–507.CrossRefGoogle Scholar
  27. Frolich, L. and Biewener, A. (1992) Kinematic and electromyographic analysis of the functional role of the body axis during terrestrial and aquatic locomotion in the salamander Ambystoma tigrinum. J. Exp. Biol. 62, 107–130.Google Scholar
  28. Fukuoka, Y., Kimura, H., and Cohen, A. (2003) Adaptive dynamic walking of a quadruped robot on irregular terrain based on biological concepts. Int. J. Robot. Res. 3–4, 187–202.CrossRefGoogle Scholar
  29. Gao, K.-Q. and Shubin, N. (2001) Late jurassic salamanders from northern china. Nature 410, 574–577.PubMedCrossRefGoogle Scholar
  30. Gillis, G. (1997) Anguiliform locomotion in an elongate salamander (siren intermedia): effects of speed on axial undulatory movements. J. Exp. Biol. 200, 767–784.PubMedGoogle Scholar
  31. Grillner, S. (1985) Neural control of vertebrate locomotion-central mechanisms and reflex interaction with special reference to the cat. In: Feedback and Motor Control in Invertebrates and Vertebrates. Barnes, W. and Gladden. M. H. (eds.) Croom Helm, London, pp. 35–56.Google Scholar
  32. Grillner, S., Buchanan, J., Wallén, P., and Brodin, L. (1988) Neural control of locmotion in lower vertebrates. In: Neural Control of Rhythmic Movements in Vertebrates. Cohen, A. H., Rossignol, S., and Grillner, S. (eds.) John Wiley & Sons, New York, pp. 1–40.Google Scholar
  33. Grillner, S., Degliana, T., Ekeberg, O., et al. (1995) Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci. 18(6), 270–279.PubMedCrossRefGoogle Scholar
  34. Grillner, S., Wallén, P., and Brodin, L. (1991) Neuronal network generating locomotor behavior in lamprey: Circuitry, transmitters, membrane properties, and simulation. Annu. Rev. Neurosci. 14, 169–199.PubMedCrossRefGoogle Scholar
  35. Guan, L., Kiemel, T., and Cohen, A. (2001) Impact of movement and movement-related feedback on the lamprey central pattern generator for locomotion. J. Exp. Biol. 204, 2361–2370.PubMedGoogle Scholar
  36. Hiraoka, A. and Kimura, H. (2002) A development of a salamander robot-design of a coupled neuromusculoskeletal system. In: Proceedings of the Annual Conference of the Robotics Society of Japan, Osaka.Google Scholar
  37. Hirose, S. and Fukushima, E. (2002) Snakes and strings: New robotic components for rescue operations. In: Experimental Robotics VIII: Proceedings of the eight International Symposium ISER02. Siciliano, B. and Paolo, D. (eds.) Springer-Verlag, Berlin, pp. 48–63.Google Scholar
  38. Ijspeert, A. (2001) A connectionist central pattern generator for the aquatic and terrestrial gaits of a simulated salamander. Biol. Cybern. 84(5), 331–348.PubMedCrossRefGoogle Scholar
  39. Ijspeert, A., Nakanishi, J., and Schaal, S. (2002) Movement imitation with nonlinear dynamical systems in humanoid robots. In: IEEE International Conference on Robotics and Automation (ICRA2002) pp. 1398–1403.Google Scholar
  40. Ijspeert, A. J., Nakanishi, J., and Schaal, S. (2003) Learning control policies for movement imitation and movement recognition. In: Neural Information Processing System 15. Becker, S. T. S. and Obermayer, K. (eds.) pp. 1547–1554.Google Scholar
  41. Kiemle, T., Gormley, K., Guan, L., Williams, T., and Cohen, A. (2003) Estimating the strength and direction of functional coupling in the lamprey spinal cord. J. Comput. Neurosci. 15, 233–245.CrossRefGoogle Scholar
  42. Kopell, N. (1995) Chains of coupled oscillators. In: The handbook of brain theory and neural networks. Arbib, M. (ed.) MIT Press, Cambridge, MA. pp. 178–183.Google Scholar
  43. Lewis, M. (1996) Self-organization of locomotory controllers in robots and animals. Doctoral dissertation, Faculty of the Graduate School, University of Southern California. (unpublished).Google Scholar
  44. McClellan, A. and Sigvardt, K. (1988) Features of entrainment of spinal pattern generators for locomotor activity in the lamprey spinal cord. J. Neurosci. 8, 133–145.PubMedGoogle Scholar
  45. McIsaac, K. and Ostrowski, J. (1999) A geometric approach to anguilliform locomotion: Simulation and experiments with an underwater eel-robot. In: Icra 1999: Proceedings of 1999 IEEE International Conference on Robotics and Automation. pp. 2843–2848.Google Scholar
  46. Ottoson, D. (1976) Morphology and physiology of muscle spindles. In: Frog neurobiology, a Handbook (Llinas, R. and Precht, W., eds.) Springer-Verlag, Berlin. pp. 643–675.Google Scholar
  47. Pratt, J., Chew, C., Torres, A., Dilworth, P., and Pratt, G. (2001) Virtual model control: An intuitive approach for bipedal locomotion. Int. J. Robot. Res. 20(2), 129–143.CrossRefGoogle Scholar
  48. Roth, G., Nishikawa, K., Naujoks-Manteuffel, C., Schmidt, A., and Wake, D. (1993) Paedomorphosis and simplification in the nervous system of salamanders. Brain Behav. Evol. 42, 137–170.PubMedGoogle Scholar
  49. Roth, G., Nishikawa, K., and Wake, D. (1997) Genome size, secondary simplification, and the evolution of the brain in salamanders. Brain Behav. Evol. 50, 50–59.PubMedGoogle Scholar
  50. Saranli, U., Buehler, M., and Koditschek, D. (2001) RHex—a simple and highly mobile hexapod robot. Int. J. Robot. Res. 20(7), 616–631.CrossRefGoogle Scholar
  51. Schroeder, D. and Egar, M. (1990) Marginal neurons in the urodele spinal cord and the associated denticulate ligaments. J. Comp. Neurol. 301, 93–103.PubMedCrossRefGoogle Scholar
  52. Székely, G. and Czéh, G. (1976) Organization of locomotion. In: Frog Neurobiology, a Handbook. Springer-Verlag, Berlin, pp. 765–792.Google Scholar
  53. Taga, G. (1998) A model of the neuro-musculo-skeletal system for anticipatory adjustment of human locomotion during obstacle avoidance. Biol. Cybern. 78(1), 9–17.PubMedCrossRefGoogle Scholar
  54. Taga, G., Yamaguchi, Y., and Shimizu, H. (1991) Self-organized control of bipedal locomotion by neural oscillators in unpredictable environment. Biol. Cybern. 65, 147–159.PubMedCrossRefGoogle Scholar
  55. Viana Di Prisco, G., Wallén, P., and Grillner, S. (1990) Synaptic effects of intraspinal stretch receptor neurons mediating movement-related feedback during locomotion. Brain Res. 530, 161–166.CrossRefGoogle Scholar
  56. Vukobratovic, M. and Borovac, B. (2004) Zeromoment point-thirty five years of life. Int. J. Hum. Robot. 1(1), 157–173.CrossRefGoogle Scholar
  57. Wallén, P., Ekeberg, O., Lansner, A., Brodin, L., Traven, H., and Grillner, S. (1992). A computer-based model for realistic simulations of neural networks II: The segmental network generating locomotor rhythmicity in the lamprey. J. Neurophys. 68, 1939–1950.Google Scholar
  58. Webb, B. (2001) Can robots make good models of biological behaviour? Behav. Brain Sci. 24(6), 1033–1050.PubMedGoogle Scholar
  59. Webb, B. (2002) Robots in invertebrate neuroscience. Nature 417, 359–363.PubMedCrossRefGoogle Scholar
  60. Wheatley, M., Edamura, M., and Stein, R. (1992) A comparison of intact and in-vitro locomotion in an adult amphibian. Exp. Brain Res. 88, 609–614.PubMedCrossRefGoogle Scholar
  61. Wilbur, C., Vorus, W., Cao, Y., and Currie, S. (2002) Neurotechnology for biomimetic robots. In: (chap. A Lamprey-Based Undulatory Vehicle). Ayers, J. Davis, J. and Rudolph, A. (eds.) Bradford/MIT Press, Cambridge, London.Google Scholar
  62. Williams, T. (1992) Phase coupling by synaptic spread in chains of coupled neuronal oscillators. Science 258, 662–665.PubMedCrossRefGoogle Scholar
  63. Williams, T. and Sigvardt, K. (1995) Spinal cord of lamprey: generation of locomotor patterns. In: The Handbook of Brain Theory and Neural Networks. Arbib, M. (ed.) MIT Press, Cambridge, London, pp. 918–921.Google Scholar
  64. Williams, T., Sigvardt, K., Kopell, N., Ermentrout, G., and Rempler, M. (1990) Forcing of coupled nonlinear oscillators: studies of intersegmental co-ordination in the lamprey locomotor central pattern generator. J. Neurophys. 64, 862–871.Google Scholar

Copyright information

© Humana Press Inc 2005

Authors and Affiliations

  • Auke Jan Ijspeert
    • 1
    Email author
  • Alessandro Crespi
    • 1
  • Jean-Marie Cabelguen
    • 2
  1. 1.Swiss Federal Institute of TechnologyLausanne (EPFL)LausanneSwitzerland
  2. 2.Inserm E 358Institut MagendieBordeauxFrance

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