The role of genetically-defined interneurons in generating the mammalian locomotor rhythm

Integrative and Comparative Biology

Volumn 51, Issue 6, 2011, Pages 903-912

  Gosgnach, Simon ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL; CONFERENCE PAPER; CYTOLOGY; ELECTROPHYSIOLOGY; GENETIC PROCEDURES; INTERNEURON; MAMMAL; MOTOR ACTIVITY; NERVE CELL INHIBITION; NERVE CELL NETWORK; NEURAL TUBE; PERIODICITY; PHYSIOLOGY; SPINAL CORD; WALKING;

ANIMALS; ELECTROPHYSIOLOGICAL PHENOMENA; GENETIC TECHNIQUES; INTERNEURONS; MAMMALS; MOTOR ACTIVITY; NERVE NET; NEURAL INHIBITION; NEURAL TUBE; PERIODICITY; SPINAL CORD; TRANSCRIPTION FACTORS; WALKING;

EID: 82255164207     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/icr022     Document Type: Conference Paper

References (93)

1. Arber S, Han B, Mendelsohn M, Smith M, Jessell TM, Sockanathan S. 1999. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23:659-74. (Pubitemid 29411557)
2. Bang AG, Goulding MD. 1996. Regulation of vertebrate neural cell fate by transcription factors. Curr Opin Neurobiol 6:25-32. (Pubitemid 26102963)
3. Bannatyne BA, Edgley SA, Hammar I, Jankowska E, Maxwell DJ. 2003. Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions. Eur J Neurosci 18:2273-84. (Pubitemid 38117400)
4. Betley JN, Wright CV, Kawaguchi Y, Erdélyi F, Szabó G, Jessell TM, Kaltschmidt JA. 2009. Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit. Cell 139:161-74.
5. Bonnot A, Morin D. 1998. Hemisegmental localisation of rhythmic networks in the lumbosacral spinal cord of neonate mouse. Brain Res 793:136-48. (Pubitemid 28294082)
6. Bouvier J, Thoby-Brisson M, Renier N, Dubreuil V, Ericson J, Champagnat J, Pierani A, Chédotal A, Fortin G. 2010. Hindbrain interneurons and axon guidance signaling critical for breathing. Nat Neurosci 13:1066-74.
7. Bracci E, Ballerini L, Nistri A. 1996. Spontaneous rhythmic bursts induced by pharmacological block of inhibition in lumbar motoneurons of the neonatal rat spinal cord. J Neurophysiol 75:640-7. (Pubitemid 26073462)
8. Bracci E, Beato M, Nistri A. 1998. Extracellular K+ induces locomotor-like patterns in the rat spinal cord in vitro: comparison with NMDA or 5-HT induced activity. J Neurophysiol 79:2643-52. (Pubitemid 28261648)
9. Briscoe J, Sussel L, Serup P, Hartigan-O'Connor D, Jessell TM, Rubenstein JL, Ericson J. 1999. Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398:622-7. (Pubitemid 29183690)
10. Brown TG. 1911. The intrinsic factors in the act of progression in the mammals. Proc Roy Soc 84:308.
11. Brownstone RM, Wilson J. 2008. Strategies for delineating spinal locomotor rhythm generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res Rev 57:65-74.
12. Burrill JD, Moran L, Goulding MD, Saueressig H. 1997. PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1+ interneurons that require PAX6 for their development. Development 124:4493-503. (Pubitemid 27519245)
13. Cazalets JR, Sqalli-Houssaini Y, Clarac F. 1992. Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol 455:187-204.
14. Cheng L, Samad OA, Xu Y, Mizuguchi R, Luo P, Shirasawa S, Goulding M, Ma Q. 2005. Lbx1 and Tlx3 are opposing switches in determining GABAergic versus glutamatergic transmitter phenotypes. Nat Neurosci 8:1510-5. (Pubitemid 41573665)
15. Clarac F, Brocard F, Vinay L. 2004. The maturation of locomotor networks. Prog Brain Res 143:57-66. (Pubitemid 37442981)
16. Cowley KC, Schmidt BJ. 1997. Regional distribution of the locomotor pattern-generating network in the neonatal rat spinal cord. J Neurophysiol 77:247-59. (Pubitemid 27053780)
17. Crone SA, et al. 2008. Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 60:70-83.
18. Crone SA, Zhong G, Harris-Warrick R, Sharma K. 2009. In mice lacking V2a interneurons, gait depends on speed of locomotion. J Neurosci 29:7098-109.
19. Dougherty KJ, Kiehn O. 2010a. Functional organization of V2a-related locomotor circuits in the rodent spinal cord. Ann NY Acad Sci 1198:85-93.
20. Dougherty KJ, Kiehn O. 2010b. Firing and cellular properties of V2a interneurons in the rodent spinal cord. J Neurosci 30:24-37.
21. Drew T, Dubuc R, Rossignol S. 1986. Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill. J Neurophysiol 55:375-401. (Pubitemid 16102858)
22. Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, van Heyningen V, Jessell TM, Briscoe J. 1997. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90:169-80. (Pubitemid 28009428)
23. Garcia-Campmany L, Stam FJ, Goulding M. 2010. From circuits to behaviour: motor networks in vertebrates. Curr Opin Neurobiol 20:116-25.
24. Garcia-Rill E, Skinner RD. 1987. The mesencephalic locomotor region. I. Activation of a medullary projection site. Brain Res 411:1-12. (Pubitemid 17084764)
25. Gosgnach S, Lanuza GM, Butt SJ, Saueressig H, Zhang Y, Velasquez T, Riethmacher D, Callaway EM, Kiehn O, Goulding M. 2006. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440:215-9. (Pubitemid 43372099)
26. Goulding M. 2009. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 10:507-18.
27. Goulding M, Lamar E. 2000. Neuronal patterning: making stripes in the spinal cord. Curr Biol 10:R565-868.
28. Goulding M, Lanuza G, Sapir T, Narayan S. 2002. The formation of sensorimotor circuits. Curr Opin Neurobiol 12:508-15. (Pubitemid 35284085)
29. Goulding M, Pfaff SL. 2005. Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr Opin Neurobiol 15:14-20. (Pubitemid 40249956)
30. Gray PA, et al. 2010. Developmental origin of preBötzinger complex respiratory neurons. J Neurosci 30:14883-95.
31. Grillner S. 1975. Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol Rev 55:247-304.
32. Grillner S. 2003. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573-86. (Pubitemid 37279129)
33. Grillner S, Dubuc R. 1988. Control of locomotion in vertebrates: spinal and supraspinal mechanisms. Adv Neurol 47:425-53.
34. Grillner S, Zangger P. 1984. The effect of dorsal root transection on the efferent motor pattern in the cat's hindlimb during locomotion. Acta Physiol Scand 120:393-405. (Pubitemid 14162606)
35. Gross MK, Dottori M, Goulding M. 2002. Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34:535-49. (Pubitemid 34628751)
36. Hägglund M, Borgius L, Dougherty KJ, Kiehn O. 2010. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evoke locomotion. Nat Neurosci 13:246-52.
37. Harris-Warrick RM. 2010. General principles of rhythmogenesis in central pattern generator networks. Prog Brain Res 187:213-22.
38. Hinckley CA, Hartley R, Wu L, Todd A, Ziskind-Conhaim L. 2005. Locomotor-like rhythms in a genetically distinct cluster of interneurons in the mammalian spinal cord. J Neurophysiol 93:1439-49. (Pubitemid 40283732)
39. Hinckley CA, Wiesner EP, Mentis GZ, Titus DJ, Ziskind- Conhaim L. 2010. Sensory modulation of locomotor-like membrane oscillations in Hb9-expressing interneurons. J Neurophysiol 103:3407-23.
40. Hochman S, Jordan LM, Schmidt BJ. 1994. TTX-resistant NMDA receptor-mediated voltage oscillations in mammalian lumbar motoneurons. J Neurophysiol 72:2559-62. (Pubitemid 24362650)
41. Jankowska E. 2001. Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol 533:31-40. (Pubitemid 32499354)
42. Jankowska E, Hammar I, Slawinska U, Maleszak K, Edgley SA. 2003. Neuronal basis of crossed actions from the reticular formation on feline hindlimb motoneurons. J Neurosci 23:1867-78. (Pubitemid 36314742)
43. Jones BE, Yang TZ. 1985. The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56-92. (Pubitemid 16202793)
44. Karunaratne A, Hargrave M, Poh A, Yamada T. 2002. GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Dev Biol 249:30-43.
45. Kiehn O. 2006. Locomotor circuits in the mammalian spinal cord. Annual Rev Neurosci 29:279-306. (Pubitemid 44476847)
46. Kiehn O, Butt SJ. 2003. Physiological, anatomical and genetic identification of CPG neurons in the developing mammalian spinal cord. Prog Neurobiol 70:347-61. (Pubitemid 37101136)
47. Kiehn O, Dougherty KJ, Hägglund M, Borgius L, Talpalar A, Restrepo CE. 2010. Probing spinal circuits controlling walking in mammals. Biochem Biophys Res Commun 396:11-8.
48. Kiehn O, Kjaerulff O. 1998. Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 860:110-29. (Pubitemid 29045964)
49. Kiehn O, Kullander K. 2004. Central pattern generators deciphered by molecular genetics. Neuron 41:317-21. (Pubitemid 38221037)
50. Kiehn O, Quinlan KA, Restrepo CE, Lundfald L, Borgius L, Talpalar AE, Endo T. 2008. Excitatory components of the mammalian locomotor CPG. Brain Res Rev 57:56-63. (Pubitemid 350213090)
51. Kjaerulff O, Kiehn O. 1996. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16:5777-94. (Pubitemid 26293400)
52. Kremer E, Lev-Tov A. 1997. Localization of the spinal network responsible for generation of hindlimb locomotion in the neonatal rat and organization of its transverse coupling system. J Neurophysiol 77:1155-70. (Pubitemid 27137016)
53. Kudo N, Yamada T. 1987. N-methyl-D,L-aspartate-induced locomotor activity in a spinal cord-hindlimb muscles preparation of the newborn rat studied in vitro. Neurosci Lett 75:43-8. (Pubitemid 17029954)
54. Kwan AC, Dietz SB, Webb WW, Harris-Warrick RM. 2009. Activity of Hb9 interneurons during fictive locomotion in mouse spinal cord. J Neurosci 29:11601-13.
55. Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M. 2004. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42:375-86. (Pubitemid 38610137)
56. Lanuza GM, Zhang Y, Velasquez T, Goulding M. 2007. Spinal V2b cells comprise a second group of inhibitory ipsilateral interneurons that participate in locomotor circuits. Program No 187.8, 2007 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2007.
57. Lundfald L, Restrepo CE, Butt SJ, Peng CY, Droho S, Endo T, Zeilhofer HU, Sharma K, Kiehn O. 2007. Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur J Neurosci 26:2989-3002. (Pubitemid 350135167)
58. Matise MP, Joyner AL. 1997. Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J Neurosci 17:7805-16. (Pubitemid 27426218)
59. Matsuyama K, Nakajima K, Mori F, Aoki M, Mori S. 2004. Lumbar commissural interneurons with reticulospinal inputs in the cat: morphology and discharge patterns during fictive locomotion. J Comp Neurol 474:546-61. (Pubitemid 38720424)
60. McCrea DA. 1998. Neuronal basis of afferent-evoked enhancement of locomotor activity. Ann NY Acad Sci 860:216-25. (Pubitemid 29045972)
61. McCrea DA, Rybak IA. 2007. Modeling the mammalian locomotor CPG: insights from mistakes and perturbations. Prog Brain Res 165:235-53. (Pubitemid 47513877)
62. Mizuguchi R, Kriks S, Cordes R, Gossler A, Ma Q, Goulding M. 2006. Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat Neurosci 9:770-8.
63. Moran-Rivard L, Kagawa T, Saueressig H, Gross MK, Burrill J, Goulding M. 2001. Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29:385-99. (Pubitemid 32206478)
64. Noga BR, Fortier PA, Kriellaars DJ, Dai X, Detillieux GR, Jordan LM. 1995. Field potential mapping of neurons in the lumbar spinal cord activated following stimulation of the mesencephalic locomotor region. J Neurosci 15:2203-17.
65. Peng CY, Yajima H, Burns CE, Zon LI, Sisodia SS, Pfaff SL, Sharma K. 2007. Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53:813-27. (Pubitemid 46389564)
66. Pierani A, Brenner-Morton S, Chiang C, Jessell TM. 1999. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97:903-15. (Pubitemid 29375049)
67. Pierani A, Moran-Rivard L, Sunshine MJ, Littman DR, Goulding M, Jessell TM. 2001. Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29:367-84. (Pubitemid 32206477)
68. Pillai A, Mansouri A, Behringer R, Westphal H, Goulding M. 2007. Lhx1 and Lhx5 maintain the inhibitoryneurotransmitter status of interneurons in the dorsal spinal cord. Development 134:357-66.
69. Quinlan KA, Kiehn O. 2007. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J Neurosci 27:6521-30. (Pubitemid 46920380)
70. Rabe G, Gezelius H, Vallstedt A, Memic F, Kullander K. 2010. Netrin-1-dependent spinal interneuron subtypes are required for the formation of left-right alternating locomotor circuitry. J Neurosci 29:15642-9.
71. Roberts A, Soffe SR, Wolf ES, Yoshida M, Zhao FY. 1998. Central circuits controlling locomotion in young frog tadpoles. Ann NY Acad Sci 860:19-34. (Pubitemid 29045957)
72. Sapir T, Geiman EJ, Wang Z, Velasquez T, Mitsui S, Yoshihara Y, Frank E, Alvarez FJ, Goulding M. 2004. Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development. J Neurosci 24:1255-64. (Pubitemid 38177032)
73. Saueressig H, Burrill J, Goulding M. 1999. Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126:4201-12. (Pubitemid 29509336)
74. Schmidt BJ, Hochman S, MacLean JN. 1998. NMDA receptor-mediated oscillatory properties: potential role for rhythm generation in the mammalian spinal cord. Ann NY Acad Sci 860:189-202. (Pubitemid 29045970)
75. Shefchyk SJ, Jell RM, Jordan LM. 1984. Reversible cooling of the brainstem reveals areas required for mesencephalic locomotor region evoked treadmill locomotion. Exp Brain Res 56:257-62. (Pubitemid 14068881)
76. Shik ML, Severin FV, Orlovskii GN. 1966. Control of walking and running by means of electric stimulation of the midbrain. Biofizika 11:659-66.
77. Smith E, Hargrave M, Yamada T, Begley CG, Little MH. 2002. Coexpression of SCL and GATA3 in the V2 interneurons of the developing mouse spinal cord. Dev Dyn 224:231-7. (Pubitemid 34569063)
78. Steeves JD, Jordan LM. 1980. Localization of a descending pathway in the spinal cord which is necessary for controlled treadmill locomotion. Neurosci Lett 20:283-8. (Pubitemid 11160065)
79. Szokol K, Glover JC, Perreault MC. 2011. Organization of functional synaptic connections between medullary reticulospinal neurons and lumbar descending commissural interneurons in the neonatal mouse. J Neurosci 31:4731-42.
80. Talpalar AE, Kiehn O. 2010. Glutamatergic mechanisms for speed control and network operation in the rodent locomotor CPG. Front Neural Circuits 4:19.
81. Tanabe Y, Jessell TM. 1996. Diversity and pattern in the developing spinal cord. Science 274:1115-23.
82. 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 98:613-28. (Pubitemid 47236019)
83. Tazerart S, Vinay L, Brocard F. 2008. The persistent sodium current generates pacemaker activities in the central pattern generator for locomotion and regulates the locomotor rhythm. J Neurosci 28:8577-89.
84. Thuret S, Moon LD, Gage FH. 2006. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7:628-43. (Pubitemid 44106745)
85. Whelan P, Bonnot A, O'Donovan MJ. 2000. Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J Neurophysiol 84:2821-33.
86. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM. 2005. Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25:5710-9.
87. Zagoraiou L, Akay T, Martin JF, Brownstone RM, Jessell TM, Miles GB. 2009. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64:645-62.
88. Zhang Y, et al. 2008. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 60:84-96.
89. Zhong G, Droho S, Crone SA, Dietz S, Kwan AC, Webb WW, Sharma K, Harris-Warrick RM. 2010. Electrophysiological characterization of V2a interneurons and their locomotorrelated activity in the neonatal mouse spinal cord. J Neurosci 30:170-82.
90. Zhong G, Masino MA, Harris-Warrick RM. 2007. Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27:4507-18. (Pubitemid 46663577)
91. Zhou Y, Yamamoto M, Engel JD. 2000. GATA2 is required for the generation of V2 interneurons. Development 127:3829-38.
92. Ziskind-Conhaim L, Mentis GZ, Wiesner EP, Titus DJ. 2010. Synaptic integration of rhythmogenic neurons in the locomotor circuitry: the case of Hb9 interneurons. Ann NY Acad Sci 1198:72-84.
93. Ziskind-Conhaim L, Wu L, Wiesner EP. 2008. Persistent sodium current contributes to induced voltage oscillations in locomotor-related hb9 interneurons in the mouse spinal cord. J Neurophysiol 100:2254-64.