Biological Cybernetics

, Volume 107, Issue 5, pp 545–564 | Cite as

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

  • Andrej BicanskiEmail author
  • Dimitri Ryczko
  • Jérémie Knuesel
  • Nalin Harischandra
  • Vanessa Charrier
  • Örjan Ekeberg
  • Jean-Marie Cabelguen
  • Auke Jan Ijspeert


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.


Salamander Locomotion Oscillators Modeling Neurobiology Robotics 



A.B. receives financial supported from the Swiss initiative in systems biology: 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.


  1. Ashley-Ross MA (1994a) Hindlimb kinematics during terrestrial locomotion in salamander (Dicamptodon tenebrosus). J Exp Biol 193:255–283Google Scholar
  2. Ashley-Ross MA (1994b) Metamorphic and speed effects on hindlimb kinematics during terrestrial locomotion in the salamander Dicamptodon tenebrosus. J Exp Biol 193:285–305PubMedGoogle Scholar
  3. Ashley-Ross MA (1995) Patterns of hind limb motor output during walking in the salamander Dicamptodon tenebrosus, with comparisons to other tetrapods. J Comp Physiol [A] 177:273–285Google Scholar
  4. Ashley-Ross MA, Lauder GV (1997) Motor patterns and kinematics during backward walking in the pacific giant salamander: evidence for novel motor output. J Neurophysiol 78:3047–3060PubMedGoogle Scholar
  5. Ashley-Ross MA, Bechtel BF (2004) Kinematics of the transition between aquatic and terrestrial locomotion in the newt Taricha torosa. J Exp Biol 207:461–474PubMedCrossRefGoogle Scholar
  6. Ashley-Ross MA, Lundin R, Johnson KL (2009) Kinematics of level terrestrial and underwater walking in the California newt, Taricha torosa. J Exp Zool A Ecol Genet Physiol 311:240–257PubMedCrossRefGoogle Scholar
  7. Azizi E, Horton JM (2004) Patterns of axial and appendicular movements during aquatic walking in the salamander Siren lacertina. Zoology 107:111–120PubMedCrossRefGoogle Scholar
  8. Bar-Gad I, Kagan I (1999) Behavior of hindbrain neurons during the transition from rest to evoked locomotion in a newt. Prog Brain Res 123:285–294PubMedCrossRefGoogle Scholar
  9. Bem T, Cabelguen J-M, Ekeberg Ö, Grillner S (2003) From swimming to walking: a single basic network for two different behaviors. Biol Cybern 88:79–90PubMedCrossRefGoogle Scholar
  10. Bennett WO, Simons RS, Brainerd EL (2001) Twisting and bending: the functional role of salamander lateral hypaxial musculature during locomotion. J Exp Biol 204:1979–1989PubMedGoogle Scholar
  11. Bicanski A, Ryczko D, Cabelguen JM, Ijspeert AJ (2011) Modeling axial spinal segments of the salamander central pattern generator for locomotion. BMC Neurosci 12(Suppl. 1):P157CrossRefGoogle Scholar
  12. Bicanski A, Ryczko D, Cabelguen JM, Ijspeert A (2012) From Lamprey to Salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander. Biol Cybern. doi: 10.1007/s00422-012-0538-y
  13. Bizzi E, Tresch M, Saltiel P (2000) New perspectives on spinal motor systems. Nat Rev Neurosci 1:101–108PubMedCrossRefGoogle Scholar
  14. Bizzi E, Cheung VCK, d’Avella A, Saltiel P, Tresch M (2008) Combining modules for movement. Brain Res Rev 57:125–133PubMedCrossRefGoogle Scholar
  15. Bowtell G, Williams T (1991) Anguiliform body dynamics: modelling the interaction between muscle activation and body curvature. Phil Trans R Soc Lond B 334:385–390Google Scholar
  16. Brändle K, Székely G (1973) The control of alternating coordination of limb pairs in the newt (Triturus vulgaris). Brain Behav Evol 8: 366–385Google Scholar
  17. Buchanan JT, Grillner S, Cullheim S, Risling M (1989) Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function. J Neurophysiol 62:59–69PubMedGoogle Scholar
  18. Buchanan JT (2001) Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog Neurobiol 63: 441–466Google Scholar
  19. Cabelguen J-M, Bourcier-Lucas C, Dubuc R (2003) Bimodal locomotion elicited by electrical stimulation of the midbrain in the salamander Notophthalmus viridescens. J Neurosci 23:2434–2439Google Scholar
  20. Cabelguen J-M, Ijspeert A, Lamarque S, Ryczko D (2010) Axial dynamics during locomotion in vertebrates: lesson from the salamander. Prog Brain Res 187:149–162Google Scholar
  21. Cangiano L, Grillner S (2003) Fast and slow locomotor burst generation in the hemispinal cord of the lamprey. J Neurophysiol 89:2931–2942PubMedCrossRefGoogle Scholar
  22. Carrier DR (1993) Action of the hypaxial muscles during walking and swimming in the salamander Dicamptodon ensatus. J Exp Biol 180:75–83Google Scholar
  23. Charrier V, Lamarque S, Ryczko D, Cabelguen J-M (2010) Kinematic and electromyographical analysis of the adaptation of locomotor movements in the salamander, Pleurodeles waltlii. 7th Forum of European Neuroscience, AmsterdamGoogle Scholar
  24. Charrier V, Cabelguen JM (2011) Fictive rhythmic motor patterns generated in tail segments of the adult salamander. Society for Neuroscience, Program 386.04, Abstr. TT15Google Scholar
  25. Chevallier S, Jan Ijspeert A (2008) Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling. Brain Res Rev 57:147–161PubMedCrossRefGoogle Scholar
  26. Chevallier S, Landry M, Nagy F, Cabelguen J-M (2004) Recovery of bimodal locomotion in the spinal-transected salamander, Pleurodeles waltlii. Eur J Neurosci 20:1995–2007PubMedCrossRefGoogle Scholar
  27. Cheng J, Stein RB, Jovanovic K, Yoshida K, Bennett DJ, Han Y (1998) Identification, localization, and modulation of neural networks for walking in the mudpuppy (Necturus maculatus) spinal cord. J Neurosci 18:4295–4304PubMedGoogle Scholar
  28. Cheng J, Jovanovic K, Aoyagi Y, Bennett DJ, Han Y, Stein RB (2002) Differential distribution of interneurons in the neural networks that control walking in the mudpuppy (Necturus maculatus) spinal cord. Exp Brain Res 145:190–198PubMedCrossRefGoogle Scholar
  29. Cheung VC, d’Avella A, Tresch MC, Bizzi E (2005) Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J Neurosci 25: 6419–6434Google Scholar
  30. Cohen AH, Rossignol S, Grillner S (1988) Neural control of rhythmic movements in vertebrates. Wiley-InterscienceGoogle Scholar
  31. Cohen AH, Ermentrout GB, Kiemel T, Kopell N, Sigvardt KA, Williams TL (1992) Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion. Trends Neurosci 15: 434–438Google Scholar
  32. Currie SN, Stein PS (1990) Cutaneous stimulation evokes long-lasting excitation of spinal interneurons in the turtle. J Neurophysiol 64: 1134–1148Google Scholar
  33. Daan S, Belterman T (1968) Lateral bending in locomotion of some lower tetrapods. Proc Ned Akad Wetten C 71:245–266Google Scholar
  34. D’Août K, Aerts P, DeVree F (1996) The timing of muscle strain and activation during steady swimming in a salamander, Ambystoma mexicanum. Neth J Zool 46:263–271CrossRefGoogle Scholar
  35. D’Avella A, Bizzi E (1998) Low dimensionality of supraspinally induced force fields. Proc Natl Acad Sci USA 95:7711–7714PubMedCrossRefGoogle Scholar
  36. Deban SM, Schilling N (2009) Activity of trunk muscles during aquatic and terrestrial locomotion in Ambystoma maculatum. J Exp Biol 212:2949–2959PubMedCrossRefGoogle Scholar
  37. Deliagina TG, Zelenin PV, Fagerstedt P, Grillner S, Orlovsky GN (2000) Activity of reticulospinal neurons during locomotion in the freely behaving lamprey. J Neurophysiol 83:853–863PubMedGoogle Scholar
  38. Delvolvé I, Bem T, Cabelguen JM (1997) Epaxial and limb muscle activity during swimming and terrestrial stepping in the adult newt, Pleurodeles waltlii. J Neurophysiol 78:638–650Google Scholar
  39. Delvolvé I, Branchereau P, Dubuc R, Cabelguen JM (1999) Fictive rhythmic motor patterns induced by NMDA in an in vitro brain stem-spinal cord preparation from an adult urodele. J Neurophysiol 82:1074–1077PubMedGoogle Scholar
  40. Dominici N, Ivanenko Y, Cappellini G, d’Avella A (2011) Locomotor primitives in newborn babies and their development. Science 334:997–999PubMedCrossRefGoogle Scholar
  41. Dubuc R (2009) Locomotor regions in the midbrain (MLR) and diencephalon (DLR). In: Binder MD, Hirokawa N, Windhorst U (eds) Encyclopedia of neuroscience. Springer, BerlinGoogle Scholar
  42. Dubuc R, Brocard F, Antri M, Fénelon K, Gariépy J-F, Smetana R, Ménard A (2008) Initiation of locomotion in lampreys. Brain Res Rev 57:172–182PubMedCrossRefGoogle Scholar
  43. Edwards JL (1977) The evolution of terrestrial locomotion. In: Hecht MK, Goody PC, Hecht BM (eds) Major patterns in vertebrate evolution. Plenum Publishing Corp, New York, pp 553–576CrossRefGoogle Scholar
  44. Eidelberg E, Walden JG, Nguyen LH (1981) Locomotor control in macaque monkeys. Brain 104:647–663PubMedCrossRefGoogle Scholar
  45. Ekeberg Ö (1993) A combined neuronal and mechanical model of fish swimming. Biol Cybern 69:363–374Google Scholar
  46. El Manira A, Tegnér J, Grillner S (1994) Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol 72:1852–1861PubMedGoogle Scholar
  47. Fagerstedt P, Orlovsky GN, Deliagina TG, Grillner S, Ullén F (2001) Lateral turns in the lamprey. II. Activity of reticulospinal neurons during the generation of fictive turns. J Neurophysiol 86:2257–2265PubMedGoogle Scholar
  48. Frolich L, 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 162:107–130Google Scholar
  49. Gillis G (1997) Anguilliform locomotion in an elongate salamander (Siren intermedia): effects of speed on axial undulatory movements. J Exp Biol 200:767–784PubMedGoogle Scholar
  50. Giszter SF, Mussa-Ivaldi FA, Bizzi E (1993) Convergent force fields organized in the frog’s spinal cord. J Neurosci 13:467–491PubMedGoogle Scholar
  51. Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Brooks VB (ed) Handbook of physiology, the nervous system. Motor control. Bethesda, Am Physiol Soc, sect. I, vol 2, pp 1179–1236Google Scholar
  52. Grillner S, McClellan A, Sigvardt K (1982) Mechanosensitive neurons in the spinal cord of the lamprey. Brain Res 235:169–173PubMedCrossRefGoogle Scholar
  53. Grillner S, Williams T, Lagerback PA (1984) The edge cell, a possible intraspinal mechanoreceptor. Science 223:500–503PubMedCrossRefGoogle Scholar
  54. Grillner S, Wallén P (1985) Central pattern generators for locomotion, with special reference to vertebrates. Annu Rev Neurosci 8:linebreak 233–261Google Scholar
  55. Grillner S, Georgopoulos AP, Jordan LM (1997) Selection and initiation of motor behavior. In: Stein PSG, Grillner S, Selverston AI, Stuart DG (eds) Neurons, networks, and motor behavior. MIT Press, Cambridge, pp. 3–19Google Scholar
  56. Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751–766PubMedCrossRefGoogle Scholar
  57. Grillner S (2011) Human locomotor circuits conform. Science 334: 912–913Google Scholar
  58. Guan L, Kiemel T, Cohen AH (2001) Impact of movement and movement-related feedback on the lamprey central pattern generator for locomotion. J Experim Biol 204:2361–2370Google Scholar
  59. Hagevik A, McClellan AD (1994) Coupling of spinal locomotor networks in larval lamprey revealed by receptor blockers for inhibitory amino acids: neurophysiology and computer modeling. J Neurophysiol 72:1810–1829PubMedGoogle Scholar
  60. Harper CE, Roberts A (1993) Spinal cord neuron classes in embryos of the smooth newt Triturus vulgaris: a horseradish peroxidase and immunocytochemical study. Philos Trans R Soc Lond B Biol Sci 340:141–160PubMedCrossRefGoogle Scholar
  61. Harishandra N, Cabelguen JM, Ekeberg O (2010) A 3D Musculo-mechanical model of the salamander for the study of different gaits and modes of locomotion. Front Neurorobot 4:112Google Scholar
  62. Harischandra N, Knuesel J, Kozlov A, Bicanski A, Cabelguen JM, Ijspeert AJ, Ekeberg Ö (2011) Sensory feedback plays a significant role in generating walking gait and in gait transition in salamanders: a simulation study. Front Neurorobot 5:3PubMedCrossRefGoogle Scholar
  63. Hill AAV, Masino MA, Calabrese RL (2003) Intersegmental coordination of rhythmic motor patterns. J Neurophysiol 90:531–538PubMedCrossRefGoogle Scholar
  64. Hubbard CS, Dolence EK, Rose JD (2010) Brainstem reticulospinal neurons are targets for corticotropin-releasing factor-Induced locomotion in roughskin newts. Horm Behav 57:237–246PubMedCrossRefGoogle Scholar
  65. Ijspeert AJ (2001) A connectionist central pattern generator for the aquatic and terrestrial gaits of a simulated salamander. Biol Cybern 84:331–348PubMedCrossRefGoogle Scholar
  66. Ijspeert AJ, Crespi A, Cabelguen J-M (2005) Simulation and robotics studies of salamander locomotion: applying neurobiological principles to the control of locomotion in robots. Neuroinf 3:171–195CrossRefGoogle Scholar
  67. Ijspeert AJ, Crespi A, Ryczko D, Cabelguen J-M (2007) From swimming to walking with a salamander robot driven by a spinal cord model. Science 315:1416–1420PubMedCrossRefGoogle Scholar
  68. Ijspeert AJ (2008) Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21:642–653PubMedCrossRefGoogle Scholar
  69. Jackson AW, Horinek DF, Boyd MR, McClellan AD (2005) Disruption of left-right reciprocal coupling in the spinal cord of larval lamprey abolishes brain-initiated locomotor activity. J Neurophysiol 94:2031–2044PubMedCrossRefGoogle Scholar
  70. Jacobson R, Hollyday MA (1982) Electrically evoked walking and fictive locomotion in the chick. J Neurophysiol 48:257–270PubMedGoogle Scholar
  71. Jovanovic K, Burke RE (2004) Morphology of brachial segments in mudpuppy (Necturus maculosus) spinal cord studied with confocal and electron microscopy. J Comp Neurol 471:361–385Google Scholar
  72. Jovanovic K, Petrov T, Stein RB (1999) Effects of inhibitory neurotransmitters on the mudpuppy (Necturus maculatus) locomotor pattern in vitro. Exp Brain Res 129:172–184Google Scholar
  73. Karakasiliotis K, Schilling N, Cabelguen JM, Ijspeert AJ (2012) How far are we in understanding salamander’s locomotion: a kinematics perspective from biology and robotics. Biol Cybern (submitted to—same issue)Google Scholar
  74. Kiemel T, Cohen AH (2001) Bending the lamprey spinal cord causes a slowly-decaying increase in the frequency of fictive swimming. Brain Res 900:57–64PubMedCrossRefGoogle Scholar
  75. Knuesel J, Ijspeert AJ (2011) Effects of muscle dynamics and proprioceptive feedback on the kinematics and CPG activity of salamander stepping. BMC Neurosci 12(Suppl. 1):P157Google Scholar
  76. Kopell N, Ermentrout GB, Williams TL (1991) On chains of oscillators forced at one end. SIAM J Appl Math 51:1397–1417CrossRefGoogle Scholar
  77. Kozlov A, Huss M, Lansner A, Kotaleski JH, Grillner S (2009) Simple cellular and network control principles govern complex patterns of motor behavior. Proc Natl Acad Sci USA 106:20027–20032Google Scholar
  78. Kozlov A, Lansner A, Grillner S, Kotaleski JH (2007) A hemicord locomotor network of excitatory interneurons: a simulation study. Biol Cybern 96(2):229–243Google Scholar
  79. Lamarque S, Ryczko D, Didier H, Cabelguen J-M (2009) Dynamics of the axial locomotor network in intact, freely moving salamanders. Neural Chall. 31st International symposium of GRSNC, MontréalGoogle Scholar
  80. Lavrov I, Cheng J (2004) Activation of NMDA receptors is required for the initiation and maintenance of walking-like activity in the mudpuppy (Necturus maculatus). Can J Physiol Pharmacol 82:637–644.Google Scholar
  81. Lavrov I, Cheng J (2008) Methodological optimization of applying neuroactive agents for the study of locomotor-like activity in the mudpuppies (Necturus maculatus). J Neurosci Methods 174:97–102Google Scholar
  82. Le Ray D, Juvin L, Ryczko D (2011) Supraspinal control of locomotion: the mesencephalic locomotor region. Prog Brain Res 188:51–70PubMedCrossRefGoogle Scholar
  83. Lemon RN (2008) Descending pathways in motor control. Annu Rev Neurosci 31:195–218PubMedCrossRefGoogle Scholar
  84. Loeb G (2001) Learning from the spinal cord. J Physiol 533:111–117PubMedCrossRefGoogle Scholar
  85. Lowry CA, Rose JD, Moore FL (1996) Corticotropin-releasing factor enhances locomotion and medullary neuronal firing in an amphibian. Horm Behav 30:50–59Google Scholar
  86. Matsushima T, Grillner S (1992) Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. J Neurophysiol 67:373–388PubMedGoogle Scholar
  87. McClellan AD (1986) Command systems for initiating locomotor responses in fish and amphibians—parallels to initiation of locomotion in mammals. In: Grillner S, Stein P, Stuart D, Forssberg H, Herman R (eds) Neurobiology of vertebrate locomotion, Wenner-Gren symposium series. MacMillan Press, London, vol 45, pp. 3–20.Google Scholar
  88. McCrea DA, Rybak IA (2008) Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57:134–146PubMedCrossRefGoogle Scholar
  89. Muller E, Buessing L, Schemmel J, Meier K (2007) Spike-frequency adapting neural ensembles: beyond mean adaptation and renewal theories. Neural Comput 19:2958–3010PubMedCrossRefGoogle Scholar
  90. Mullins OJ, Hackett JT, Buchanan JT, Friesen OW (2011) Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model system. Prog Neurobiol 93:244–269PubMedCrossRefGoogle Scholar
  91. Mussa-Ivaldi FA, Giszter SF, Bizzi E (1994) Linear combinations of primitives in vertebrate motor control. Proc Natl Acad Sci USA 91:7534–7538PubMedCrossRefGoogle Scholar
  92. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16:265–297PubMedCrossRefGoogle Scholar
  93. Pearson K, Ekeberg Ö, Büschges A (2006) Assessing sensory function in locomotor systems using neuro-mechanical simulations. Trends Neurosci 29:625–631PubMedCrossRefGoogle Scholar
  94. Peters SE, Goslow GE Jr (1983) From salamanders to mammals: continuity in musculoskeletal function during locomotion. Brain Behav Evol 22:191–197PubMedCrossRefGoogle Scholar
  95. Rauscent A (2008) Remaniements fonctionnels des réseaux locomoteurs spinaux au cours du développement de l’amphibien Xenopus laevis en métamorphose. PhD thesis, Université Bordeaux 1, BordeauxGoogle Scholar
  96. Roos P (1964) Lateral bending in newt locomotion. Proc Ned Akad Wetten C 67:223–232Google Scholar
  97. Rossignol S, Chau C, Brustein E, Giroux N, Bouyer L, Barbeau H, Reader TA (1998) Pharmacological activation and modulation of the central pattern generator for locomotion in the cat. Ann N Y Acad Sci 860:346–359Google Scholar
  98. Rossignol S, Dubuc R, Gossard JP (2006) Dynamic sensorimotor interactions in locomotion. Physiol Rev 86:89–154PubMedCrossRefGoogle Scholar
  99. Ryczko D (2008) Dynamique de l’organisation fonctionnelle des réseaux locomoteurs chez la salamandre: du module rythmogène à une palette de modes locomoteurs. PhD thesis, Université de Bordeaux 2, BordeauxGoogle Scholar
  100. Ryczko D, Lamarque S, Didier H, Cabelguen JM (2009) Dynamics of the axial locomotor network in the isolated spinal cord of the salamander. Society for Neuroscience, Program 565.8, Abstr. EE6Google Scholar
  101. Ryczko D, Charrier V, Ijspeert A, Cabelguen JM (2010a) Segmental oscillators in axial motor circuits of the salamander: distribution and bursting mechanisms. J Neurophysiol 104:2677–2692Google Scholar
  102. Ryczko D, Dubuc R, Cabelguen J-M (2010b) Rhythmogenesis in axial locomotor networks: an interspecies comparison. Prog Brain Res 187:189–211Google Scholar
  103. Saltiel P, Tresch MC, Bizzi E (1998) Spinal cord modular organization and rhythm generation: an NMDA iontophoretic study in the frog. J Neurophysiol 80:2323–2339PubMedGoogle Scholar
  104. Schroeder DM, Egar MW (1990) Marginal neurons in the urodele spinal cord and the associated denticulate ligaments. J Comp Neurol 301:93–103PubMedCrossRefGoogle Scholar
  105. Shik ML, Severin FV, Orlovskii GN (1966) Control of walking and running by means of electric stimulation of the midbrain. Biofizika 11:659–666PubMedGoogle Scholar
  106. Skinner RD, Garcia-Rill E (1984) The mesencephalic locomotor region (MLR) in the rat. Brain Res 323:385–389PubMedCrossRefGoogle Scholar
  107. Steeves JD, Sholomenko GN, Webster DMS (1987) Stimulation of the pontomedullary reticular formation initiates locomotion in decerebrate birds. Brain Res 401:205–212PubMedCrossRefGoogle Scholar
  108. Székely G, Czéh G (1976) Organisation of Locomotion. In: Llinás RR, Precht W, Capranica RR (eds) Frog neurobiology: a handbook, Springer Verlag, Berlin, pp. 765–792Google Scholar
  109. Székely G, Czéh G, Vörös G (1969) The activity pattern of limb muscles in freely moving normal and deafferented newts. Exp Brain Res 9:53–72PubMedCrossRefGoogle Scholar
  110. Tresch MC, Bizzi E (1999) Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activiated by low threshold cutaneous stimulation. Exp Brain Res 129:401–416PubMedCrossRefGoogle Scholar
  111. Tresch MC, Kiehn O (2002) Synchronization of motor neurons during locomotion in the neonatal rat: predictors and mechanisms. J Neurosci 22:9997–10008PubMedGoogle Scholar
  112. Tytell E, Hsu C, Williams T, Cohen AH, Fauci LJ (2010) Interactions between internal forces, body stiffness, and fluid environment in a neuromechanical model of lamprey swimming. Proc Natl Acad Sci USA 107:19832–19837PubMedCrossRefGoogle Scholar
  113. Uematsu K, Todo T (1997) Identification of the midbrain locomotor nuclei and their descending pathways in the teleost carp. Cyprinus carpio Brain Res 773:1–7CrossRefGoogle Scholar
  114. van den Kieboom J (2009) Biped locomotion and stability—a practical approach. Masters thesis, Department of Artificial Intelligence, University of Groningen, the NetherlandsGoogle Scholar
  115. Wallén P, Williams TL (1984) Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. J Physiol 347:225–239PubMedGoogle Scholar
  116. Wallén P, Grillner S (1997) Central pattern generators and their interaction with sensory feedback. Proc Am Control Conf 5:2851–2855Google Scholar
  117. Wallén P, Ekeberg O, Lansner A, Brodin L, Tråvén H, Grillner S (1992) A computer-based model for realistic simulations of neural networks. II. The segmental network generating locomotor rhythmicity in the lamprey. J Neurophysiol 68:1939–1950 Google Scholar
  118. Wheatley M, Edamura M, Stein RB (1992) A comparison of intact and in vitro locomotion in an adult amphibian. Exp Brain Res 88:609–614Google Scholar
  119. Wheatley M, Jovanovic K, Stein RB, Lawson V (1994) The activity of interneurons during locomotion in the in vitro necturus spinal cord. J Neurophysiol 71:2025–2032Google Scholar
  120. Wheatley M, Stein RB (1992) An in vitro preparation of the mudpuppy for simultaneous intracellular and electromyographic recording during locomotion. J Neurosci Methods 42:129–137Google Scholar
  121. Williams TL, Sigvardt KA, Kopell N, Ermentrout GB, Remler MP (1990) Forcing of coupled nonlinear oscillators: studies of intersegmental coordination in the lamprey locomotor central pattern generator. J Neurophysiol 64:862–871Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Andrej Bicanski
    • 1
    Email author
  • Dimitri Ryczko
    • 2
  • Jérémie Knuesel
    • 1
  • Nalin Harischandra
    • 3
    • 4
  • Vanessa Charrier
    • 5
  • Örjan Ekeberg
    • 6
  • Jean-Marie Cabelguen
    • 5
  • Auke Jan Ijspeert
    • 1
  1. 1.Biorobotics Laboratory, School of EngineeringÉcole Polytechnique Fédérale de LausanneLausanneSwitzerland
  2. 2.Groupe de Recherche sur le Système Nerveux Central, Département de PhysiologieUniversité de MontréalMontréalCanada
  3. 3.Department of Computational BiologyKTH Royal Institute of Technology, School of Computer Science and EngineeringStockholmSweden
  4. 4.Department of Biological Cybernetics, Faculty of BiologyUniversity of BielefeldBielefeldGermany
  5. 5.INSERM U862, Neurocentre Magendie, Motor System Diseases GroupUniversité BordeauxBordeaux CedexFrance
  6. 6.Department of Computational BiologyKTH Royal Institute of Technology, School of Computer Science and CommunicationStockholmSweden

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