Neuroscience Bulletin

, Volume 29, Issue 4, pp 467–476 | Cite as

Anatomical and electrophysiological plasticity of locomotor networks following spinal transection in the salamander

  • Jean-Marie Cabelguen
  • Stéphanie Chevallier
  • Ianina Amontieva-Potapova
  • Céline Philippe
Review

Abstract

Recovery of locomotor behavior following spinal cord injury can occur spontaneously in some vertebrates, such as fish, urodele amphibians, and certain reptiles. This review provides an overview of the current status of our knowledge on the anatomical and electrophysiological changes occurring within the spinal cord that lead to, or are associated with the re-expression of locomotion in spinally-transected salamanders. A better understanding of these processes will help to devise strategies for restoring locomotor function in mammals, including humans.

Keywords

salamander spinal cord locomotor recovery regeneration 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. [1]
    Carter C, Clark A, Spencer G, Carlone R. Cloning and expression of a retinoic acid receptor beta2 subtype from the adult newt: evidence for an early role in tail and caudal spinal cord regeneration. Dev Dyn 2011, 240: 2613–2625.PubMedCrossRefGoogle Scholar
  2. [2]
    Chernoff EA, Stocum DL, Nye HL, Cameron JA. Urodele spinal cord regeneration and related processes. Dev Dyn 2003, 226: 295–307.PubMedCrossRefGoogle Scholar
  3. [3]
    Ferreira LM, Floriddia EM, Quadrato G, Di Giovanni S. Neural regeneration: lessons from regenerating and nonregenerating systems. Mol Neurobiol 2012, 46: 227–241.PubMedCrossRefGoogle Scholar
  4. [4]
    Ferretti P, Zhang F, O’Neill P. Changes in spinal cord regenerative ability through phylogenesis and development: lessons to be learnt. Dev Dyn 2003, 226: 245–256.PubMedCrossRefGoogle Scholar
  5. [5]
    Mercer SE, Cheng CH, Atkinson DL, Krcmery J, Guzman CE, Kent DT, et al. Multi-tissue microarray analysis identifies a molecular signature of regeneration. PLoS one 2012, 7: e52375.PubMedCrossRefGoogle Scholar
  6. [6]
    Zhang F, Ferretti P, Clarke JD. Recruitment of postmitotic neurons into the regenerating spinal cord of urodeles. Dev Dyn 2003, 226: 341–348.PubMedCrossRefGoogle Scholar
  7. [7]
    Zukor KA, Kent DT, Odelberg SJ. Meningeal cells and glia establish a permissive environment for axon regeneration after spinal cord injury in newts. Neural Dev 2011, 6: 1.PubMedCrossRefGoogle Scholar
  8. [8]
    Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999, 49: 377–391.PubMedCrossRefGoogle Scholar
  9. [9]
    Schwab JM, Bernard F, Moreau-Fauvarque C, Chedotal A. Injury reactive myelin/oligodendrocyte-derived axon growth inhibition in the adult mammalian central nervous system. Brain Res Brain Res Rev 2005, 49: 295–299.PubMedCrossRefGoogle Scholar
  10. [10]
    Schwab ME, Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 1996, 76: 319–370.PubMedGoogle Scholar
  11. [11]
    Schwab ME. Increasing plasticity and functional recovery of the lesioned spinal cord. Prog Brain Res 2002, 137: 351–359.PubMedCrossRefGoogle Scholar
  12. [12]
    Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 2003, 4: 573–586.PubMedCrossRefGoogle Scholar
  13. [13]
    Rossignol S, Dubuc R, Gossard JP. Dynamic sensorimotor interactions in locomotion. Physiol Rev 2006, 86: 89–154.PubMedCrossRefGoogle Scholar
  14. [14]
    Bradbury EJ, McMahon SB. Spinal cord repair strategies: why do they work? Nat Rev Neurosci 2006, 7: 644–653.PubMedCrossRefGoogle Scholar
  15. [15]
    Lurie DI, Selzer ME. Axonal regeneration in the adult lamprey spinal cord. J Comp Neurol 1991, 306: 409–416.PubMedCrossRefGoogle Scholar
  16. [16]
    Sirbulescu RF, Zupanc GK. Spinal cord repair in regeneration-competent vertebrates: adult teleost fish as a model system. Brain Res Rev 2011, 67: 73–93.PubMedCrossRefGoogle Scholar
  17. [17]
    Butler EG, Ward MB. Reconstitution of the spinal cord after ablation in adult Triturus. Dev Biol 1967, 15: 464–486.PubMedCrossRefGoogle Scholar
  18. [18]
    Piatt J. Regeneration of the spinal cord in the salamander. J Exp Zool 1955, 29: 177–208.CrossRefGoogle Scholar
  19. [19]
    Chevallier S, Landry M, Nagy F, Cabelguen JM. Recovery of bimodal locomotion in the spinal-transected salamander, Pleurodeles waltlii. Eur J Neurosci 2004, 20: 1995–2007.PubMedCrossRefGoogle Scholar
  20. [20]
    Davis BM, Ayers JL, Koran L, Carlson J, Anderson MC, Simpson SB Jr. Time course of salamander spinal cord regeneration and recovery of swimming: HRP retrograde pathway tracing and kinematic analysis. Exp Neurol 1990, 108: 198–213.PubMedCrossRefGoogle Scholar
  21. [21]
    Davis BM, Duffy MT, Simpson SB Jr. Bulbospinal and intraspinal connections in normal and regenerated salamander spinal cord. Exp Neurol 1989, 103: 41–51.PubMedCrossRefGoogle Scholar
  22. [22]
    Doyle LM, Stafford PP, Roberts BL. Recovery of locomotion correlated with axonal regeneration after a complete spinal transection in the eel. Neuroscience 2001, 107: 169–179.PubMedCrossRefGoogle Scholar
  23. [23]
    McClellan AD. Functional regeneration and restoration of locomotor activity following spinal cord transection in the lamprey. Prog Brain Res 1994, 103: 203–217.PubMedCrossRefGoogle Scholar
  24. [24]
    Zhang L, Palmer R, McClellan AD. Increase in descending brain-spinal cord projections with age in larval lamprey: implications for spinal cord injury. J Comp Neurol 2002, 447: 128–137.PubMedCrossRefGoogle Scholar
  25. [25]
    Cohen AH, Kiemel T, Pate V, Blinder J, Guan L. Temperature can alter the function outcome of spinal cord regeneration in larval lampreys. Neuroscience 1999, 90: 957–965.PubMedCrossRefGoogle Scholar
  26. [26]
    Yin HS, Selzer ME. Axonal regeneration in lamprey spinal cord. J Neurosci 1983, 3: 1135–1144.PubMedGoogle Scholar
  27. [27]
    Armstrong J, Zhang L, McClellan AD. Axonal regeneration of descending and ascending spinal projection neurons in spinal cord-transected larval lamprey. Exp Neurol 2003, 180: 156–166.PubMedCrossRefGoogle Scholar
  28. [28]
    Clarke JD, Alexander R, Holder N. Regeneration of descending axons in the spinal cord of the axolotl. Neurosci Lett 1988, 89: 1–6.PubMedCrossRefGoogle Scholar
  29. [29]
    Davis GR Jr, McClellan AD. Long distance axonal regeneration of identified lamprey reticulospinal neurons. Exp Neurol 1994, 127: 94–105.PubMedCrossRefGoogle Scholar
  30. [30]
    Edgerton VR, Leon RD, Harkema SJ, Hodgson JA, London N, Reinkensmeyer DJ, et al. Retraining the injured spinal cord. J Physiol 2001, 533: 15–22.PubMedCrossRefGoogle Scholar
  31. [31]
    Rehermann MI, Marichal N, Russo RE, Trujillo-Cenoz O. Neural reconnection in the transected spinal cord of the freshwater turtle Trachemys dorbignyi. J Comp Neurol 2009, 515: 197–214.PubMedCrossRefGoogle Scholar
  32. [32]
    Arshavsky YuI, Gelfand IM, Orlovsky GN, Pavlova GA, Popova LB. Origin of signals conveyed by the ventral spinocerebellar tract and spino-reticulo-cerebellar pathway. Exp Brain Res 1984, 54: 426–431.PubMedCrossRefGoogle Scholar
  33. [33]
    Orsal D, Perret C, Cabelguen JM. Comparison between ventral spinocerebellar and rubrospinal activities during locomotion in the cat. Behav Brain Res 1988, 28: 159–162.PubMedCrossRefGoogle Scholar
  34. [34]
    Vinay L, Grillner S. Spino-bulbar neurons convey information to the brainstem about different phases of the locomotor cycle in the lamprey. Brain Res 1992, 582: 134–138.PubMedCrossRefGoogle Scholar
  35. [35]
    Stensaas LJ. Regeneration in the spinal cord of the newt notophthalmus (triturus) pyrrhogaster. in: Kao CC, Bunge RP, Reier PJ (Eds.). Spinal Cord Reconstruction. New York: Raven Press, 1983: 121–149.Google Scholar
  36. [36]
    Bunt SM, Fill-Moebs P. Selection of pathways by regenerating spinal cord fiber tracts. Brain Res 1984, 318: 307–311.PubMedGoogle Scholar
  37. [37]
    Beattie MS, Bresnahan JC, Lopate G. Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs. J Neurobiol 1990, 21: 1108–1122.PubMedCrossRefGoogle Scholar
  38. [38]
    Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 2004, 7: 269–277.PubMedCrossRefGoogle Scholar
  39. [39]
    Chevallier S, Jan Ijspeert A, Ryczko D, Nagy F, Cabelguen JM. Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling. Brain Res Rev 2008, 57: 147–161.PubMedCrossRefGoogle Scholar
  40. [40]
    Delvolve I, Branchereau P, Dubuc R, Cabelguen JM. Fictive rhythmic motor patterns induced by NMDA in an in vitro brain stem-spinal cord preparation from an adult urodele. J Neurophysiol 1999, 82: 1074–1077.PubMedGoogle Scholar
  41. [41]
    Ryczko D, Charrier V, Ijspeert A, Cabelguen JM. Segmental oscillators in axial motor circuits of the salamander: distribution and bursting mechanisms. J Neurophysiol 2010, 104: 2677–2692.PubMedCrossRefGoogle Scholar
  42. [42]
    Wheatley M, Stein RB. An in vitro preparation of the mudpuppy for simultaneous intracellular and electromyographic recording during locomotion. J Neurosci Methods 1992, 42: 129–137.PubMedCrossRefGoogle Scholar
  43. [43]
    Bicanski A, Ryczko D, Knuesel J, Harischandra N, Charrier V, Ekeberg O, et al. Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics. Biol Cybern 2013.Google Scholar
  44. [44]
    Ijspeert AJ, Crespi A, Ryczko D, Cabelguen JM. From swimming to walking with a salamander robot driven by a spinal cord model. Science 2007, 315: 1416–1420.PubMedCrossRefGoogle Scholar
  45. [45]
    Frolich LM, Biewener AA. 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 1992, 162: 107–130.Google Scholar
  46. [46]
    Delvolve I, Bem T, Cabelguen JM. Epaxial and limb muscle activity during swimming and terrestrial stepping in the adult newt, Pleurodeles waltl. J Neurophysiol 1997, 78: 638–650.PubMedGoogle Scholar
  47. [47]
    Becker T, Wullimann MF, Becker CG, Bernhardt RR, Schachner M. Axonal regrowth after spinal cord transection in adult zebrafish. J Comp Neurol 1997, 377: 577–595.PubMedCrossRefGoogle Scholar
  48. [48]
    Mackler SA, Selzer ME. Regeneration of functional synapses between individual recognizable neurons in the lamprey spinal cord. Science 1985, 229: 774–776.PubMedCrossRefGoogle Scholar
  49. [49]
    Wood MR, Cohen MJ. Synaptic regeneration in identified neurons of the lamprey spinal cords. Science 1979, 206: 344–347.PubMedCrossRefGoogle Scholar
  50. [50]
    Cohen AH, Mackler SA, Selzer ME. Behavioral recovery following spinal transection: functional regeneration in the lamprey CNS. Trends Neurosci 1988, 11: 227–231.PubMedCrossRefGoogle Scholar
  51. [51]
    McClellan AD. Locomotor recovery in spinal-transected lamprey: regenerated spinal coordinating neurons and mechanosensory inputs couple locomotor activity across a spinal lesion. Neuroscience 1990, 35: 675–685.PubMedCrossRefGoogle Scholar
  52. [52]
    Pearson KG. Plasticity of neuronal networks in the spinal cord: modifications in response to altered sensory input. Prog Brain Res 2000, 128: 61–70.PubMedCrossRefGoogle Scholar
  53. [53]
    Pearson KG, Rossignol S. Fictive motor patterns in chronic spinal cats. J Neurophysiol 1991, 66: 1874–1887.PubMedGoogle Scholar
  54. [54]
    Doyle LM, Roberts BL. Exercise enhances axonal growth and functional recovery in the regenerating spinal cord. Neuroscience 2006, 141: 321–327.PubMedCrossRefGoogle Scholar
  55. [55]
    Belanger M, Drew T, Provencher J, Rossignol S. A comparison of treadmill locomotion in adult cats before and after spinal transection. J Neurophysiol 1996, 76: 471–491.PubMedGoogle Scholar
  56. [56]
    Orlovsky GN, Deliagina TG, Grillner S. Neural Control of Locomotion. New York: Oxford University Press, 1999.Google Scholar
  57. [57]
    Grillner S. The spinal locomotor CPG: a target after spinal cord injury. Prog Brain Res 2002, 137: 97–108.PubMedCrossRefGoogle Scholar
  58. [58]
    Branchereau P, Rodriguez JJ, Delvolve I, Abrous DN, Le Moal M, Cabelguen JM. Serotonergic systems in the spinal cord of the amphibian urodele Pleurodeles waltl. J Comp Neurol 2000, 419: 49–60.PubMedCrossRefGoogle Scholar
  59. [59]
    Jovanovic K, Petrov T, Greer JJ, Stein RB. Serotonergic modulation of the mudpuppy (Necturus maculatus) locomotor pattern in vitro. Exp Brain Res 1996, 111: 57–67.PubMedCrossRefGoogle Scholar
  60. [60]
    Schmidt BJ, Jordan LM. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 2000, 53: 689–710.PubMedCrossRefGoogle Scholar
  61. [61]
    Lotto B, Upton L, Price DJ, Gaspar P. Serotonin receptor activation enhances neurite outgrowth of thalamic neurones in rodents. Neurosci Lett 1999, 269: 87–90.PubMedCrossRefGoogle Scholar
  62. [62]
    Schwartz JP. Neurotransmitters as neurotrophic factors: a new set of functions. Int Rev Neurobiol 1992, 34: 1–23.PubMedCrossRefGoogle Scholar
  63. [63]
    Jordan LM, Schmidt BJ. Propriospinal neurons involved in the control of locomotion: potential targets for repair strategies? Prog Brain Res 2002, 137: 125–139.PubMedCrossRefGoogle Scholar
  64. [64]
    Miles GB, Hartley R, Todd AJ, Brownstone RM. Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci U S A 2007, 104: 2448–2453.PubMedCrossRefGoogle Scholar
  65. [65]
    Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL. Synaptic control of motoneuronal excitability. Physiol Rev 2000, 80: 767–852.PubMedGoogle Scholar
  66. [66]
    Russo RE, Hounsgaard J. Dynamics of intrinsic electrophysiological properties in spinal cord neurones. Prog Biophys Mol Biol 1999, 72: 329–365.PubMedCrossRefGoogle Scholar
  67. [67]
    Pearson KG. Neural adaptation in the generation of rhythmic behavior. Annu Rev Physiol 2000, 62: 723–753.PubMedCrossRefGoogle Scholar
  68. [68]
    Quinlan KA, Placas PG, Buchanan JT. Cholinergic modulation of the locomotor network in the lamprey spinal cord. J Neurophysiol 2004, 92: 1536–1548.PubMedCrossRefGoogle Scholar
  69. [69]
    Fok M, Stein RB. Effects of cholinergic and noradrenergic agents on locomotion in the mudpuppy (Necturus maculatus). Exp Brain Res 2002, 145: 498–504.PubMedCrossRefGoogle Scholar
  70. [70]
    Chevallier S, Nagy F, Cabelguen JM. Cholinergic control of excitability of spinal motoneurones in the salamander. J Physiol 2006, 570: 525–540.PubMedCrossRefGoogle Scholar
  71. [71]
    Chevallier S, Nagy F, Cabelguen JM. Muscarinic control of the excitability of hindlimb motoneurons in chronic spinaltransected salamanders. Eur J Neurosci 2008, 28: 2243–2253.PubMedCrossRefGoogle Scholar
  72. [72]
    Brownstone RM, Jordan LM, Kriellaars DJ, Noga BR, Shefchyk SJ. On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Exp Brain Res 1992, 90: 441–455.PubMedCrossRefGoogle Scholar
  73. [73]
    Schmidt BJ. Afterhyperpolarization modulation in lumbar motoneurons during locomotor-like rhythmic activity in the neonatal rat spinal cord in vitro. Exp Brain Res 1994, 99: 214–222.PubMedCrossRefGoogle Scholar
  74. [74]
    Miles GB, Sillar KT. Neuromodulation of vertebrate locomotor control networks. Physiology (Bethesda) 2011, 26: 393–411.CrossRefGoogle Scholar
  75. [75]
    Parish CL, Beljajeva A, Arenas E, Simon A. Midbrain dopaminergic neurogenesis and behavioural recovery in a salamander lesion-induced regeneration model. Development 2007, 134: 2881–2887.PubMedCrossRefGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jean-Marie Cabelguen
    • 1
  • Stéphanie Chevallier
    • 1
  • Ianina Amontieva-Potapova
    • 1
  • Céline Philippe
    • 1
  1. 1.Neurocentre MagendieINSERM U 862 — Bordeaux UniversityBordeaux CedexFrance

Personalised recommendations