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Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics

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Abstract

Vertebrate animals exhibit impressive locomotor skills. These locomotor skills are due to the complex interactions between the environment, the musculo-skeletal system and the central nervous system, in particular the spinal locomotor circuits. We are interested in decoding these interactions in the salamander, a key animal from an evolutionary point of view. It exhibits both swimming and stepping gaits and is faced with the problem of producing efficient propulsive forces using the same musculo-skeletal system in two environments with significant physical differences in density, viscosity and gravitational load. Yet its nervous system remains comparatively simple. Our approach is based on a combination of neurophysiological experiments, numerical modeling at different levels of abstraction, and robotic validation using an amphibious salamander-like robot. This article reviews the current state of our knowledge on salamander locomotion control, and presents how our approach has allowed us to obtain a first conceptual model of the salamander spinal locomotor networks. The model suggests that the salamander locomotor circuit can be seen as a lamprey-like circuit controlling axial movements of the trunk and tail, extended by specialized oscillatory centers controlling limb movements. The interplay between the two types of circuits determines the mode of locomotion under the influence of sensory feedback and descending drive, with stepping gaits at low drive, and swimming at high drive.

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Notes

  1. Henceforth the following distinctions are made between locomotor modes (e.g., swimming vs. stepping) and between gaits. The locomotor mode of stepping encompasses (i) at slow speeds, a sequential walking gait, where one foot is lifted off the ground at a time. The order in which the feet are lifted defines the further subdivision in lateral sequence walk (ipsilateral hindlimb follows the ipsilateral forelimb) and diagonal sequence walk (contralateral hindlimb follows the ipsilateral forelimb). (ii) At higher speeds, a walking trot gait, where diagonally opposite feet are lifted roughly simultaneously off the ground. At even higher speeds the walking trot turns into a running trot, with short flight phases (Daan and Belterman 1968; Carrier 1993; Ashley-Ross 1994a).

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Acknowledgments

A.B. receives financial supported from the Swiss initiative in systems biology: SystemsX.ch. D. R. receives salary support from the Groupe de Recherche sur le Système Nerveux Central (GRSNC) and the Fonds de la Recherche en Santé du Québec (FRSQ). N.H. acknowledges funding by the Swedish International Development Cooperation Agency. J.K., V.C., Ö.E., A.J.I. and J.-M.C. acknowledge support from the European Community (LAMPETRA Grant: FP7-ICT-2007-1-216100). J.-M.C. further receives support from the Fondation pour la Recherche Médicale (DBC 20101021008). The assistance of H. Didier and S. Lamarque in some experiments is gratefully acknowledged. The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Biorobotics Laboratory, School of Engineering, École Polytechnique Fédérale de Lausanne, Station 14, 1015 , Lausanne, Vaud, Switzerland

    Andrej Bicanski, Jérémie Knuesel & Auke Jan Ijspeert

  2. Groupe de Recherche sur le Système Nerveux Central, Département de Physiologie, Université de Montréal, Montréal, QC, H3C 3J7, Canada

    Dimitri Ryczko

  3. Department of Computational Biology, KTH Royal Institute of Technology, School of Computer Science and Engineering, Stockholm, Sweden

    Nalin Harischandra

  4. Department of Biological Cybernetics, Faculty of Biology, University of Bielefeld, Bielefeld, Germany

    Nalin Harischandra

  5. INSERM U862, Neurocentre Magendie, Motor System Diseases Group, Université Bordeaux, 146 rue Leo Saignat, 33077 , Bordeaux Cedex, France

    Vanessa Charrier & Jean-Marie Cabelguen

  6. Department of Computational Biology, KTH Royal Institute of Technology, School of Computer Science and Communication, Stockholm, Sweden

    Örjan Ekeberg

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  1. Andrej Bicanski
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  2. Dimitri Ryczko
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  3. Jérémie Knuesel
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  4. Nalin Harischandra
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  5. Vanessa Charrier
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  7. Jean-Marie Cabelguen
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  8. Auke Jan Ijspeert
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Correspondence to Andrej Bicanski.

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This article forms part of a special issue of Biological Cybernetics entitled “Lamprey, Salamander Robots and Central Nervous System”.

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Bicanski, A., Ryczko, D., Knuesel, J. et al. Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Biol Cybern 107, 545–564 (2013). https://doi.org/10.1007/s00422-012-0543-1

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  • DOI: https://doi.org/10.1007/s00422-012-0543-1

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