Biological Cybernetics

, Volume 107, Issue 5, pp 565–587 | Cite as

From lamprey to salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander

  • Andrej BicanskiEmail author
  • Dimitri Ryczko
  • Jean-Marie Cabelguen
  • Auke Jan Ijspeert
Original Paper


The evolutionary transition from water to land required new locomotor modes and corresponding adjustments of the spinal “central pattern generators” for locomotion. Salamanders resemble the first terrestrial tetrapods and represent a key animal for the study of these changes. Based on recent physiological data from salamanders, and previous work on the swimming, limbless lamprey, we present a model of the basic oscillatory network in the salamander spinal cord, the spinal segment. Model neurons are of the Hodgkin–Huxley type. Spinal hemisegments contain sparsely connected excitatory and inhibitory neuron populations, and are coupled to a contralateral hemisegment. The model yields a large range of experimental findings, especially the NMDA-induced oscillations observed in isolated axial hemisegments and segments of the salamander Pleurodeles waltlii. The model reproduces most of the effects of the blockade of AMPA synapses, glycinergic synapses, calcium-activated potassium current, persistent sodium current, and \(h\)-current. Driving segments with a population of brainstem neurons yields fast oscillations in the in vivo swimming frequency range. A minimal modification to the conductances involved in burst-termination yields the slower stepping frequency range. Slow oscillators can impose their frequency on fast oscillators, as is likely the case during gait transitions from swimming to stepping. Our study shows that a lamprey-like network can potentially serve as a building block of axial and limb oscillators for swimming and stepping in salamanders.


Locomotion Central pattern generator Segmental oscillators Salamander Lamprey 



A. B. receives financial supported from the Swiss initiative in systems biology: J.-M.C. receives grants from the European Community (LAMPETRA Grant: FP7-ICT-2007-1-216100) and the Fondation pour la Recherche Médicale (DBC 20101021008). 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). A. J. I. acknowledges support from the European Community (LAMPETRA Grant: FP7-ICT-2007-1-216100). A. B. acknowledges Jeremie Knüsel for critical comments on the manuscript and Daniele Colangelo for IT support; further more Richard Naud, Skander Mensi, Christian Pozzorini and Andrea Prunotto for fruitful discussions.


  1. Antri M, Fénelon K, Dubuc R (2009) The contribution of synaptic inputs to sustained depolarizations in reticulospinal neurons. J Neurosci 29:1140–1151PubMedGoogle Scholar
  2. Bar-Gad I, Kagan I, Shik ML (1999) Behavior of hindbrain neurons during the transition from rest to evoked locomotion in a newt. Prog Brain Res 123:285–294PubMedGoogle Scholar
  3. Bem T, Cabelguen J-M, Ekeberg Ö, From swimming to walking: a single basic network for two different behaviors. Biol Cybern 88:79–90.Google Scholar
  4. Berg RW, Alaburda A, Hounsgaard J (2007) Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315:390–393PubMedGoogle Scholar
  5. Bédard C, Kröger H, Destexhe A (2004) Modeling extracellular field potentials and the frequency-filtering properties of extracellular space. Biophys J 86:1829–1842PubMedGoogle Scholar
  6. Bicanski A, Ryczko D, Knuesel J, Harischandra N, Charrier V, Ekeberg Ö, Cabelguen J-M, Ijspeert AJ (2012) Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Biol Cybern. doi: 10.1007/s00422-012-543-1
  7. Bischofberger J, Schild D (1995) Different spatial patterns of [Ca2+] increase caused by N- and L-type Ca2+ channel activation in frog olfactory bulb neurones. J Physiol 487(Pt 2):305–317PubMedGoogle Scholar
  8. Bhatt DH, McLean DL, Hale ME, Fetcho JR (2007) Grading movement strength by changes in firing intensity versus recruitment of spinal interneurons. Neuron 53:91–102PubMedGoogle Scholar
  9. Bloodgood BL, Sabatini BL (2007) Nonlinear regulation of unitary synaptic signals by CaV2.3 voltage-sensitive calcium channels located in dendritic spines. Neuron 53:249–260PubMedGoogle Scholar
  10. Branchereau P, Rodriguez JJ, Delvolvé I, Abrous DN, Le Moal M, Cabelguen JM (2000) Serotonergic systems in the spinal cord of the amphibian urodele Pleurodeles waltl. J Comp Neurol 419:49–60PubMedGoogle Scholar
  11. Brocard F, Ryczko D, Fénelon K, Hatem R, Gonzales D, Auclair F, Dubuc R (2010) The transformation of a unilateral locomotor command into a symmetrical bilateral activation in the brainstem. J Neurosci 30:523–533PubMedGoogle Scholar
  12. Brocard F, Dubuc R (2003) Differential contribution of reticulospinal cells to the control of locomotion induced by the mesencephalic locomotor region. J Neurophysiol 90:1714–1727Google Scholar
  13. Brodin L, Grillner S, Dubuc R, Ohta Y, Kasicki S, Hökfelt T (1988) Reticulospinal neurons in lamprey: transmitters, synaptic interactions and their role during locomotion. Arch Ital Biol 126:317– 345PubMedGoogle Scholar
  14. Brodin L, Traven H, Lansner A (1991) Computer simulations of n-methyl-d-aspartate receptor-induced membrane properties in a neuron model. J Neurophysiol 66:473–484PubMedGoogle Scholar
  15. Buchanan J (1982) Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J Neurophysiol. 47:5Google Scholar
  16. Buchanan JT, Grillner S, Cullheim S, Risling M (1989) Identification of excitatory inter-neurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function. J Neurophysiol 62:59–69PubMedGoogle Scholar
  17. Buchanan JT, Grillner S (1987) Newly identified “glutamate interneurons” and their role in locomotion in the lamprey spinal cord. Science 236:312–314PubMedGoogle Scholar
  18. Buchanan JT, McPherson DR (1995) The neuronal network for locomotion in the lamprey spinal cord: evidence for the involvement of commissural interneurons. J Physiol Paris 89(4—-6):221–233PubMedGoogle Scholar
  19. Buchanan JT (2011) Spinal locomotor inputs to individually identified reticulospinal neurons in the lamprey. J Neurophysiol 106:2346–2357PubMedGoogle Scholar
  20. Butera R, Rinzel J (1999) Models of respiratory rhythm generation in the pre-Bötzinger complex. I. Bursting pacemaker neurons. J Neurophysiol 82:382–397PubMedGoogle Scholar
  21. Butera RJ, Rinzel J, Smith JC (1999) Models of respiratory rhythm generation in the pre-Bötzinger complex. II. Populations of coupled pacemaker neurons. J Neurophysiol 82:398–415PubMedGoogle Scholar
  22. Butt SJ, Kiehn O (2003) Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38:953–963PubMedGoogle Scholar
  23. 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 23:2434–2439PubMedGoogle Scholar
  24. Cabelguen J-M, Ijspeert A, Lamarque S, Ryczko D (2010) Axial dynamics during locomotion in vertebrates: lesson from the salamander. Prog Brain Res 187:149–162PubMedGoogle Scholar
  25. Cangiano L, Wallén P, Grillner S (2002) Role of apamin-sensitive KCa channels for reticulospinal synaptic transmission to motoneuron and for the after hyperpolarization. J Neurophysiol 88:289–299PubMedGoogle Scholar
  26. Cangiano L, Grillner S (2003) Fast and slow locomotor burst generation in the hemispinal cord of the lamprey. J Neurophysiol 89(6):2931–2942PubMedGoogle Scholar
  27. Cangiano L, Grillner S (2005) Mechanisms of rhythm generation in a spinal locomotor network deprived of crossed connections: the lamprey hemicord. J Neurosci 25:923–935PubMedGoogle Scholar
  28. Cangiano L, Hill RH, Grillner S (2012) The hemisegmental locomotor network revisited. Neuroscience 210:33–37PubMedGoogle Scholar
  29. 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 145:190–198PubMedGoogle Scholar
  30. Chevallier S, Jan Ijspeert A, Ryczko D, Nagy F, Cabelguen J-M (2008a) Organisation of the spinal central pattern generators for locomotion in the salamander: Biology and modelling. Brain Res Rev 57:147–161PubMedGoogle Scholar
  31. Chevallier S, Landry M, Nagy F, Cabelguen J-M (2004) Recovery of bimodal locomotion in the spinal-transected salamander, Pleurodeles waltlii. Eur J Neurosci 20:1995–2007PubMedGoogle Scholar
  32. Chevallier S, Nagy F, Cabelguen J-M (2006) Cholinergic control of excitability of spinal motoneurones in the salamander. J Physiol 570:525–540PubMedGoogle Scholar
  33. Chevallier S, Nagy F, Cabelguen J-M (2008b) Muscarinic control of the excitability of hindlimb motoneurons in chronic spinal-transected salamanders. Eur J Neurosci 28:2243–2253PubMedGoogle Scholar
  34. Cohen AH, Rossignol S, Grillner S (1988) Neural control of rhythmic movements in vertebrates. Wiley, New York 1Google Scholar
  35. Dale N, Roberts A (1985) Dual-component amino-acid-mediated synaptic potentials—excitatory drive for swimming in xenopus embryos. J Physiol 363:35–59PubMedGoogle Scholar
  36. Daun S, Rubin JE, Rybak IA (2009) Control of oscillation periods and phase durations in half-center central pattern generators: a comparative mechanistic analysis. J Comput Neurosci 27:3–36PubMedGoogle Scholar
  37. Davis BM, Duffy MT, Simpson SB (1989) Bulbospinal and intraspinal connections in normal and regenerated salamander spinal cord. Exp Neurol 103:41–51PubMedGoogle Scholar
  38. Dayan P, Abbott LF (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems. MIT Press, CambridgeGoogle Scholar
  39. Delvolvé I, Bem T, Cabelguen JM (1997) Epaxial and limb muscle activity during swimming and terrestrial stepping in the adult newt, Pleurodeles waltl. J Neurophysiol 78:638–650PubMedGoogle Scholar
  40. 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
  41. Dubuc R, Grillner S (1989) The role of spinal-cord inputs in modulating the activity of reticulospinal neurons during fictive locomotion in the lamprey. Brain Res 483:196–200PubMedGoogle Scholar
  42. Einum J (2004) Reticulospinal neurons receive direct spinobulbar inputs during locomotor activity in lamprey. J Neurophysiol 92:1384–1390PubMedGoogle Scholar
  43. Einum JF, Buchanan JT (2006a) Membrane potential oscillations in reticulospinal and spinobulbar neurons during locomotor activity. J Neurophysiol 94:273–281Google Scholar
  44. Einum JF, Buchanan JT (2006b) Spinobulbar neurons in lamprey: cellular properties and synaptic interactions. J Neurophysiol 96:2042–2055PubMedGoogle Scholar
  45. Ekeberg Ö, Wallén P, Lansner A, Tråvén H (1991) A computer based model for realistic simulations of neural networks. Biol Cybern 65:81–90PubMedGoogle Scholar
  46. Ekeberg Ö (1993) A combined neuronal and mechanical model of fish swimming. Biol Cybern 69:363–374Google Scholar
  47. 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 Neurophys 72(4):1852–1861Google Scholar
  48. El Manira A, Pombal M, Grillner S (1997) Diencephalic projection to reticulospinal neurons involved in the initiation of locomotion in adult lampreys Lampetra fluviatilis. J Comp Neurol 389:603–616PubMedGoogle Scholar
  49. Faber ESL, Delaney AJ, Sah P (2005) SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat Neurosci 8:635–641PubMedGoogle Scholar
  50. Faber ESL (2010) Functional interplay between NMDA receptors, SK channels and voltage-gated Ca2+ channels regulates synaptic excitability in the medial prefrontal cortex. J Physiol 588:1281–1292PubMedGoogle Scholar
  51. Falgairolle M, de Seze M, Juvin L, Morin D, Cazalets J-R (2006) Coordinated network functioning in the spinal cord: an evolutionary perspective. J Physiol Paris 100:304–316PubMedGoogle Scholar
  52. Fetcho JR, McLean DL (2010) Some principles of organization of spinal neurons underlying locomotion in zebrafish and their implications. Ann NY Acad Sci 1198:94–104PubMedGoogle Scholar
  53. Frolich L, Biewener A (1992) Kinematic and electromyographic analysis of the function-al-role of the body axis during terrestrial and aquatic locomotion in the salamander Ambystoma tigrinum. J Exp Biol 162:107–130Google Scholar
  54. Gabriel JP, Ausborn J, Ampatzis K, Mahmood R, Eklöf-Ljunggren E, El Manira A (2010) Principles governing recruitment of motoneurons during swimming in zebrafish. Nature 14:93–99Google Scholar
  55. Gao KQ, Shubin NH (2001) Late Jurassic salamanders from northern China. Nature 410:574–577PubMedGoogle Scholar
  56. Gerstner W, Kistler W (2002) Spiking neuron models. Cambridge University Press, CambridgeGoogle Scholar
  57. Grashow R, Brookings T, Marder E (2009) Reliable neuromodulation from circuits with variable underlying structure. Proc Natl Acad Sci 106:11742–11746PubMedGoogle Scholar
  58. Grillner S, McClellan A, Sigvardt K (1982) Mechanosensitive neurons in the spinal-cord of the lamprey. Brain Res 235–1:169–173Google Scholar
  59. Grillner S, Wallén P (1985) Central pattern generators for locomotion, with special reference to vertebrates. Annu Rev Neurosci. 8:233– 261Google Scholar
  60. Grillner S, Williams T, Lagerback PA (1984) The edge cell, a possible intraspinal mechanoreceptor. Science 223–4635:500–503Google Scholar
  61. Grillner S, Buchanan JT, Lansner A (1988) Simulation of the segmental burst generating network for locomotion in lamprey. Neurosci Lett 89:31–35PubMedGoogle Scholar
  62. Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573–586PubMedGoogle Scholar
  63. Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751–766PubMedGoogle Scholar
  64. 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 Ser B 340(1291):141–160Google Scholar
  65. 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 5:3PubMedGoogle Scholar
  66. Hellgren J, Grillner S, Lansner A (1992) Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons. Biol Cybern 68:1–13PubMedGoogle Scholar
  67. Hoffman N, Parker D (2010) Lesioning alters functional properties in isolated spinal cord hemisegmental networks. Neuroscience 168(3):732–743.Google Scholar
  68. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544PubMedGoogle Scholar
  69. Hubbard CS, Dolence EK, Rose JD (2010) Brainstem reticulospinal neurons are targets for corticotropin-releasing factor-induced locomotion in roughskin newts. Horm Behav 57:237–246PubMedGoogle Scholar
  70. Huss M, Lansner A, Wallén P, el Manira A, Grillner S, Kotaleski JH (2007) Roles of ionic currents in lamprey CPG neurons: a modeling study. J Neurophysiol 97:2696–2711PubMedGoogle Scholar
  71. Huss M, Wang D, Trané C, Wikström M, Hellgren Kotaleski J (2008) An experimentally constrained computational model of NMDA oscillations in lamprey CPG neurons. J Comput Neurosci 25:108–121PubMedGoogle Scholar
  72. Ijspeert AJ (2001) A connectionist central pattern generator for the aquatic and terrestrial gaits of a simulated salamander. Biol Cybern 84:331–348PubMedGoogle Scholar
  73. Ijspeert AJ, Crespi A, Cabelguen J-M (2005) Simulation and robotics studies of sala-mander locomotion: applying neurobiological principles to the control of locomotion in robots. Neuroinformatics 3:171–195PubMedGoogle Scholar
  74. 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 315:1416–1420PubMedGoogle Scholar
  75. Ijspeert AJ (2008) Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21:642–653PubMedGoogle Scholar
  76. Izhikevich EM (2007) Dynamical systems in neuroscience. MIT Press, CambridgeGoogle Scholar
  77. Jovanovic K, Petrov T, Greer JJ, Stein RB (1996) Serotonergic modulation of the mudpuppy (Necturus maculatus) locomotor pattern in vitro. Exp Brain Res 111:57–67PubMedGoogle Scholar
  78. Jovanovic K, Petrov T, Stein RB (1999) Effects of inhibitory neurotransmitters on the mudpuppy (Necturus maculatus) locomotor pattern in vitro. Exp Brain Res 129:172–184 Google Scholar
  79. Jovanovic K, Burke RE (2004) Morphology of brachial segments in mudpuppy (Necturus maculatus) spinal cord studied with confocal and electron microscopy. J Comp Neurol 471:361–385PubMedGoogle Scholar
  80. Kahn J, Roberts A (1982) Experiments on the central pattern generator for swimming in amphibian embryos. Philos Trans R Soc Lond B Biol Sci 296: 229–243Google Scholar
  81. Katz P, Harris-Warrick R (1999) The evolution of neuronal circuits underlying species-specific behavior. Curr Opin Neurobiol 9:628–633PubMedGoogle Scholar
  82. Kiehn O, Kjaerulff O, Tresch MC, Harris-Warrick RM (2000) Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord. Brain Res Bull 53:649–659PubMedGoogle Scholar
  83. Kimura Y, Okamura Y, Higashijima S (2006) alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J Neurosci 26:5684–5697PubMedGoogle Scholar
  84. Kinkhabwala A, Riley M, Koyama M, Monen J, Satou C, Kimura Y, Higashijima S-I, Fetcho J (2011) A structural and functional ground plan for neurons in the hindbrain of zebrafish. Proc Natl Acad Sci 108:1164–1169PubMedGoogle Scholar
  85. Kotaleski JH, Grillner S, Lansner A (1999a) Neural mechanisms potentially contributing to the intersegmental phase lag in lamprey. I. Segmental oscillations dependent on reciprocal inhibition. Biol Cybern 81:317–330PubMedGoogle Scholar
  86. Kotaleski JH, Lansner A, Grillner S (1999b) Neural mechanisms potentially contributing to the intersegmental phase lag in lamprey. II. Hemisegmental oscillations produced by mutually coupled excitatory neurons. Biol Cybern 81:299–315PubMedGoogle Scholar
  87. 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 106:20027–20032PubMedGoogle Scholar
  88. Kozlov AK, Lansner A, Grillner S, Kotaleski JH (2007) A hemicord locomotor network of excitatory interneurons: a simulation study. Biol Cybern 96:229–243Google Scholar
  89. Li W, Soffe S, Wolf E, Roberts A (2006) Persistent responses to brief stimuli: feedback excitation among brainstem neurons. J Neurosci 26:4026–4035PubMedGoogle Scholar
  90. Li W-C, Sautois B, Roberts A, Soffe SR (2007) Reconfiguration of a vertebrate motor network: specific neuron recruitment and context-dependent synaptic plasticity. J Neurosci 27:12267–12276PubMedGoogle Scholar
  91. Liao J, Fetcho JR (2009) Shared versus specialized glycinergic spinal interneurons in axial motor circuits of larval zebrafish. J Neurosci 28:12982–12992Google Scholar
  92. Llinás R (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305:171–195PubMedGoogle Scholar
  93. Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242:1654–1664PubMedGoogle Scholar
  94. Lin MT, Luján R, Watanabe M, Adelman JP, Maylie J (2008) SK2 channel plasticity contributes to LTP at Schaffer collateral-CA1 synapses. Nat Neurosci 11(2):170–177PubMedGoogle Scholar
  95. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ (2004) Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92:1566–1576PubMedGoogle Scholar
  96. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613–7624PubMedGoogle Scholar
  97. Magistretti J, Alonso A (1999) Biophysical properties and slow voltage-dependent inactivation of a sustained sodium current in entorhinal cortex layer-II principal neurons: a whole-cell and single-channel study. J Gen Physiol 114:491–509PubMedGoogle Scholar
  98. Mahmood R, Restrepo CE, El Manira A (2009) Transmitter phenotypes of commissural interneurons in the lamprey spinal cord. Neuroscience 164(3):1057–1067PubMedGoogle Scholar
  99. 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 67–2:373–388Google Scholar
  100. McCrea DA, Rybak IA (2008) Organization of mammalian locomotor rhythm and pattern generation. Brain Res Rev 57(1):134–146PubMedGoogle Scholar
  101. McLean DL, Fan J, Higashijima S-I, Hale ME, Fetcho JR (2007) A topographic map of recruitment in spinal cord. Nature 446: 71–75PubMedGoogle Scholar
  102. McLean DL, Masino MA, Koh IYY, Lindquist WB, Fetcho JR (2008) Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 11:1419–1429PubMedGoogle Scholar
  103. McPherson DR, Buchanan JT, Kasicki S (1994) Effects of strychnine on fictive swimming in the lamprey: evidence for glycinergic inhibition, discrepancies with model predictions, and novel modulatory rhythms. J Comp Physiol A 175:311–321PubMedGoogle Scholar
  104. Mulholland PJ (2012) K(Ca)\(_2\) channels: novel therapeutic targets for treating alcohol withdrawal and escalation of alcohol consumption. Alcohol 46(4):309–315Google Scholar
  105. Mullins OJ, Hackett JT, Buchanan JT, Friesen WO (2011) Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model systems. Prog Neurobiol 93(2):244–269PubMedGoogle Scholar
  106. Munoz A, Munoz M, González A, tenDonkelaar H (1997) Spinal ascending pathways in amphibians: cells of origin and main targets. J Comp Neurol 378:205–228PubMedGoogle Scholar
  107. Nanou E, El Manira A (2007) A postsynaptic negative feedback mediated by coupling between AMPA receptors and Na+-activated K+ channels in spinal cord neurones. Eur J Neurosci 25(2):445–450PubMedGoogle Scholar
  108. Nanou E, Kyriakatos A (2008) Na+-mediated coupling between AMPA receptors and KNa channels shapes synaptic transmission. Proc Natl Acad Sci 52:20941–20946Google Scholar
  109. Ngo-Anh TJ, Bloodgood BL, Lin M, Sabatini BL, Maylie J, Adelman JP (2005) SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nat Neurosci 8:642–649PubMedGoogle Scholar
  110. Nieuwenhuys R, ten Donkelaar HJ, Nicholson C, Smeets WJAJ (1998) The central nervous system of vertebrates, 3 volume cased set with poster book. Springer, New YorkGoogle Scholar
  111. Ohta Y, Grillner S (1989) Mono-synaptic excitatory amino-acid transmission from the posterior rhombencephalic reticular nucleus to spinal neurons involved in the control of locomotion in lamprey. J Neurophysiol 62:1079–1089PubMedGoogle Scholar
  112. Orlovsky G, Deliagina T, Grillner S, Orlovskii G (1999) Neuronal control of locomotion: from mollusc to man. Oxford University Press, New YorkGoogle Scholar
  113. Ovsepian SV, Vesselkin NP (2006) Serotonergic modulation of synaptic transmission and action potential firing in frog motoneurons. Brain Res 1102:71–77PubMedGoogle Scholar
  114. Pape HC (1996) Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58:299–327PubMedGoogle Scholar
  115. Parker D, Grillner S (2000) The activity-dependent plasticity of segmental and intersegmental synaptic connections in the lamprey spinal cord. Eur J Neurosci 12:2135–2146PubMedGoogle Scholar
  116. Perrier JF, Tresch MC (2004) Recruitment of motor neuronal persistent inward currents shapes withdrawal reflexes in the frog. J Physiol 562(2):507–520PubMedGoogle Scholar
  117. Prinz AA, Bucher D, Marder E (2004) Similar network activity from disparate circuit parameters. Nat Neurosci 7(12):1345–1352PubMedGoogle Scholar
  118. Ritter D, Bhatt D, Fetcho J (2001) In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements. J Neurosci 21:8956–8965PubMedGoogle Scholar
  119. Roberts A, Tunstall MJ (1990) Mutual re-excitation with post-inhibitory rebound: a simulation study on the mechanisms for locomotor rhythm generation in the spinal cord of xenopus embryos. Eur J Neurosci 2:11–23PubMedGoogle Scholar
  120. Roberts A, Perrins R (1995) Positive feedback as a general mechanism for sustaining rhythmic and non-rhythmic activity. J Physiol Paris 89:241–248Google Scholar
  121. Roberts A, Li WC, Soffe SR (2010) How neurons generate behavior in a hatchling amphibian tadpole: an outline. Front Behav Neurosci 4:16Google Scholar
  122. Rybak IA, Shevtsova NA, Lafreniere-Roula M, McCrea DA (2006) Modelling spinal circuitry involved in locomotor pattern generation: insights from deletions during fictive locomotion. J Physiol 577:617–639PubMedGoogle Scholar
  123. 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. EE6.Google Scholar
  124. 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
  125. Ryczko D, Dubuc R, Cabelguen J-M (2010b) Rhythmogenesis in axial locomotor networks: an interspecies comparison. Prog Brain Res 187:189–211Google Scholar
  126. Satou C, Kimura Y, Kohashi T, Horikawa K, Takeda H, Oda Y, Higashijima S-I (2009) Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish. J Neurosci 29:6780–6793PubMedGoogle Scholar
  127. Schroeder DM, Egar MW (1990) Marginal neurons in the urodele spinal cord and the associated denticulate ligaments. J Comp Neurol 301:93–103Google Scholar
  128. Shen W, Slaughter MM (1999) Metabotropic GABA receptors facilitate L-type and inhibit N-type calcium channels in single salamander retinal neurons. J Physiol 516(Pt 3):711–718PubMedGoogle Scholar
  129. Sirota MG, Di Prisco GV, Dubuc R (2000) Stimulation of the mesencephalic locomotor region elicits controlled swimming in semi-intact lampreys. Eur J Neurosci 12:4081–4092PubMedGoogle Scholar
  130. Soffe SR (1989) Roles of glycinergic inhibition and n-methyl-d-aspartate receptor mediated excitation in the locomotor rhythmicity of one half of the xenopus embryo central nervous system. Eur J Neurosci 1:561–571PubMedGoogle Scholar
  131. Stafstrom CE, Schwindt PC, Crill WE (1982) Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro. Brain Res 236:221–226PubMedGoogle Scholar
  132. Stephenson-Jones M, Samuelsson E, Ericsson J, Robertson B, Grillner S (2011) Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr Biol 21:1081–1091PubMedGoogle Scholar
  133. Stocker M (2004) Ca2+-activated K+ channels: molecular determinants and function of the SK family. Nat Rev Neurosci 5:758–770 Google Scholar
  134. Tazerart S, Viemari JC, Darbon P, Vinay L, Brocard F (2007) Contribution of persistent sodium current to locomotor pattern generation in neonatal rats. J Neurophysiol 98:613–628PubMedGoogle Scholar
  135. Tegnér J, Hellgren-Kotaleski J, Lansner A, Grillner S (1997) Low-voltage-activated calcium channels in the lamprey locomotor network: simulation and experiment. J Neuro-physiol 77:1795–1812Google Scholar
  136. Tråvén HG, Brodin L, Lansner A, Ekeberg Ö, Wallén P, Grillner S (1993) Computer simulations of NMDA and non-NMDA receptor-mediated synaptic drive: sensory and su-praspinal modulation of neurons and small networks. J Neurophysiol 70:695–709PubMedGoogle Scholar
  137. Ullström M, Kotaleski JH, Tegnér J, Aurell E, Grillner S, Lansner A (1998) Activity-dependent modulation of adaptation produces a constant burst proportion in a model of the lamprey spinal locomotor generator. Biol Cybern 79:1–14Google Scholar
  138. Vinay L, Grillner S (1993) The spino-reticulo-spinal loop can slow down the NMDA-activated spinal locomotor network in lamprey. Neuroreport 4:609–612PubMedGoogle Scholar
  139. Wallén P, Ekeberg Ö, Lansner A (1992) A computer-based model for realistic simulations of neural networks. II. The segmental network generating locomotor rhythmicity in the lamprey. J Neurophysiol 68:1939–1950PubMedGoogle Scholar
  140. Wallén P, Grillner S (1997) Central pattern generators and their interaction with sensory feedback. Proc Am Control Conf 5:2851–2855Google Scholar
  141. Wallén P, Robertson B, Cangiano L, Löw P, Bhattacharjee A, Kaczmarek LK, Grillner S (2007) Sodium-dependent potassium channels of a slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons. J Physiol (London) 585(1):75–90Google Scholar
  142. Wang D, Grillner S, Wallén P (2011) 5-HT and dopamine modulates CaV1.3 calcium channels involved in postinhibitory rebound in the spinal network for locomotion in lam-prey. J Neurophysiol 105:1212–1224PubMedGoogle Scholar
  143. Williams T, Grillner S, Smoljaninov V, Wallén P, Kashin S, Rossignol S (1989) Locomotion in lamprey and trout—the relative timing of activation and movement. J Exp Biol 143:559–566Google Scholar
  144. Zhong G, Masino MA, Harris-Warrick RM (2007) Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27:4507–4518PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Andrej Bicanski
    • 1
    Email author
  • Dimitri Ryczko
    • 2
  • Jean-Marie Cabelguen
    • 3
  • 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.INSERM U862—Neurocentre Magendie, Motor System Diseases Team, Université de BordeauxBordeaux CedexFrance

Personalised recommendations