Abstract
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.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Ashley-Ross, M. (1994a) Hindlimb kinematics during terrestrial locomotion in a salamander (dicampton tenebrosus). J. Exp. Biol. 193,255–283.
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.
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.
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.
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.
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.
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.
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).
Buchanan, J. (1992) Neural network simulations of coupled locomotor oscillators in the lamprey spinal cord. Biol. Cybern. 66, 367–374.
Buchanan, J. and Grillner, S. (1987) Newly identified ‘glutamate interneurons’ and their role in locomotion in the lamprey spinal cord. Science 236, 312–314.
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.
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.
Carrier, D. (1993) Action of the hypaxial muscles during walking and swimming in the salamander dicamptodon ensatus. J. Exp. Biol. 180, 75–63.
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.
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.
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.
Collins, J. and Richmond. (1994) Hard-wired central pattern generators for quadrupedal locomotion. Biol. Cybern. 71, 375–385.
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.
Crespi, A., Badertscher, A., Guignard, A., and Ijspeert, A. (2005b) AmphiBot I: an amphibious snake-like robot. Robot. Auton. Syst. (In press)
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.
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.
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.
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.
Ekeberg, O. (1993) A combined neuronal and mechanical model of fish swimming. Biol. Cybern. 69, 363–374.
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.
Ermentrout, B. and Kopell, N. (1994) Inhibition-produced patterning in chains of coupled nonlinear oscillators. SIAM J. Appl. Math. 54(2), 478–507.
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.
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.
Gao, K.-Q. and Shubin, N. (2001) Late jurassic salamanders from northern china. Nature 410, 574–577.
Gillis, G. (1997) Anguiliform locomotion in an elongate salamander (siren intermedia): effects of speed on axial undulatory movements. J. Exp. Biol. 200, 767–784.
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.
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.
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.
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.
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.
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.
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.
Ijspeert, A. (2001) A connectionist central pattern generator for the aquatic and terrestrial gaits of a simulated salamander. Biol. Cybern. 84(5), 331–348.
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.
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.
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.
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.
Lewis, M. (1996) Self-organization of locomotory controllers in robots and animals. Doctoral dissertation, Faculty of the Graduate School, University of Southern California. (unpublished).
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.
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.
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.
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.
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.
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.
Saranli, U., Buehler, M., and Koditschek, D. (2001) RHex—a simple and highly mobile hexapod robot. Int. J. Robot. Res. 20(7), 616–631.
Schroeder, D. and Egar, M. (1990) Marginal neurons in the urodele spinal cord and the associated denticulate ligaments. J. Comp. Neurol. 301, 93–103.
Székely, G. and Czéh, G. (1976) Organization of locomotion. In: Frog Neurobiology, a Handbook. Springer-Verlag, Berlin, pp. 765–792.
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.
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.
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.
Vukobratovic, M. and Borovac, B. (2004) Zeromoment point-thirty five years of life. Int. J. Hum. Robot. 1(1), 157–173.
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.
Webb, B. (2001) Can robots make good models of biological behaviour? Behav. Brain Sci. 24(6), 1033–1050.
Webb, B. (2002) Robots in invertebrate neuroscience. Nature 417, 359–363.
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.
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.
Williams, T. (1992) Phase coupling by synaptic spread in chains of coupled neuronal oscillators. Science 258, 662–665.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ijspeert, A.J., Crespi, A. & Cabelguen, JM. Simulation and robotics studies of salamander locomotion. Neuroinform 3, 171–195 (2005). https://doi.org/10.1385/NI:3:3:171
Issue Date:
DOI: https://doi.org/10.1385/NI:3:3:171