Dorsally derived spinal interneurons in locomotor circuits

Annals of the New York Academy of Sciences

Volumn 1279, Issue 1, 2013, Pages 32-42

  Vallstedt, Anna ^a   Kullander, Klas ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Central pattern generator; Dmrt3; Eph; Netrin; Neuronal network; Spinal cord

Indexed keywords

EPHRIN A4; EPHRIN B3; NETRIN; NETRIN 1; TRANSCRIPTION FACTOR PAX7;

ARTICLE; CELL FATE; CELL POPULATION; CENTRAL PATTERN GENERATOR; GAIT; GENE SEQUENCE; INTERNEURON; LIMB MOVEMENT; LOCOMOTION; MOTOR COORDINATION; MOTOR PERFORMANCE; NERVE FIBER; NONHUMAN; PROTEIN EXPRESSION; SPINAL CORD NERVE CELL;

EID: 84875606395     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06801.x     Document Type: Article

References (79)

1. Goulding, M. et al. 2002. The formation of sensorimotor circuits. Curr. Opin. Neurobiol. 12: 508-515.
2. Grillner, S. 2006. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52: 751-766.
3. Kiehn, O. & K. Kullander . 2004. Central pattern generators deciphered by molecular genetics. Neuron 41: 317-321.
4. Pearson, K.G. 1993. Common principles of motor control in vertebrates and invertebrates. Annu. Rev. Neurosci. 16: 265-297.
5. Kullander, K. 2005. Genetics moving to neuronal networks. Trends Neurosci. 28: 239-247.
6. Brownstone, R.M. & J.M. Wilson . 2008. Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res. Rev. 57: 64-76.
7. Grillner, S. 2003. The motor infrastructure: from ion channels to neuronal networks. Nat. Rev. Neurosci. 4: 573-586.
8. Kiehn, O. 2006. Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29: 279-306.
9. McCrea, D.A. & I.A. Rybak . 2008. Organization of mammalian locomotor rhythm and pattern generation. Brain Res. Rev. 57: 134-146.
10. Kjaerulff, O. & O. Kiehn . 1996. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J. Neurosci. 16: 5777-5794.
11. Alaynick, W.A., T.M. Jessell & S.L. Pfaff . 2011. SnapShot: spinal cord development. Cell 146: 178-178 e171.
12. Bermingham, N.A. et al. 2001. Proprioceptor pathway development is dependent on Math1. Neuron 30: 411-422.
13. Gross, M.K., M. Dottori & M. Goulding . 2002. Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34: 535-549.
14. Lanuza, G.M. et al. 2004. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42: 375-386.
15. Moran-Rivard, L. et al. 2001. Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29: 385-399.
16. Pierani, A. et al. 2001. Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29: 367-384.
17. Rabe, N. et al. 2009. Netrin-1-dependent spinal interneuron subtypes are required for the formation of left-right alternating locomotor circuitry. J. Neurosci. 29: 15642-15649.
18. Dai, X. et al. 2005. Localization of spinal neurons activated during locomotion using the c-fos immunohistochemical method. J. Neurophysiol. 93: 3442-3452.
19. Dai, Y. et al. 2009. Electrophysiological and pharmacological properties of locomotor activity-related neurons in cfos-EGFP mice. J. Neurophysiol. 102: 3365-3383.
20. Avraham, O. et al. 2009. Transcriptional control of axonal guidance and sorting in dorsal interneurons by the Lim-HD proteins Lhx9 and Lhx1. Neural. Develop. 4: 21.
21. Helms, A.W. & J.E. Johnson . 1998. Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development 125: 919-928.
22. Müller, T. et al. 2002. The homeodomain factor lbx1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34: 551-562.
23. Tripodi, M., A.E. Stepien & S. Arber . 2011. Motor antagonism exposed by spatial segregation and timing of neurogenesis. Nature 479: 61-66.
24. Kennedy, T.E. et al. 1994. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78: 425-435.
25. Serafini, T. et al. 1996. Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87: 1001-1014.
26. Wéber, I. et al. 2007. Neurotransmitter systems of commissural interneurons in the lumbar spinal cord of neonatal rats. Brain Res. 1178: 65-72.
27. Gezelius, H. et al. 2006. Role of glutamate in locomotor rhythm generating neuronal circuitry. J. Physiol. 100: 297-303.
28. Wallén-Mackenzie, A. et al. 2006. Vesicular glutamate transporter 2 is required for central respiratory rhythm generation but not for locomotor central pattern generation. J. Neurosci. 26: 12294-12307.
29. Wallen-Mackenzie, A., H. Wootz & H. Englund . 2010. Genetic inactivation of the vesicular glutamate transporter 2 (VGLUT2) in the mouse: what have we learnt about functional glutamatergic neurotransmission? Upsala J. Med. Sci. 115: 11-20.
30. Cohen, A.H. & R.M. Harris-Warrick . 1984. Strychnine eliminates alternating motor output during fictive locomotion in the lamprey. Brain Res. 293: 164-167.
31. Cowley, K.C. & B.J. Schmidt . 1995. Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J. Neurophysiol. 74: 1109-1117.
32. Grillner, S. & P. Wallen . 1980. Does the central pattern generation for locomotion in lamprey depend on glycine inhibition? Acta Physiol. Scand. 110: 103-105.
33. Jankowska, E. & B.R. Noga . 1990. Contralaterally projecting lamina VIII interneurones in middle lumbar segments in the cat. Brain Res. 535: 327-330.
34. Soffe, S.R., J.D. Clarke & A. Roberts . 1984. Activity of commissural interneurons in spinal cord of Xenopus embryos. J. Neurophysiol. 51: 1257-1267.
35. Harrison, P.J., E. Jankowska & D. Zytnicki . 1986. Lamina VIII interneurones interposed in crossed reflex pathways in the cat. J. Physiol. 371: 147-166.
36. Jankowska, E. et al. 2005. Functional differentiation and organization of feline midlumbar commissural interneurones. J. Physiol. 565: 645-658.
37. Rabe Bernhardt, N. et al. 2012. DCC mediated axon guidance of spinal interneurons is essential for normal locomotor central pattern generator function. Develop. Biol. 366: 279-289.
38. Kullander, K. et al. 2003. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 299: 1889-1892.
39. Filosa, A. et al. 2009. Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nature Neurosci. 12: 1285-1292.
40. Kullander, K. et al. 2001. Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 29: 73-84.
41. Keller, C. et al. 2004. Pax3:Fkhr interferes with embryonic Pax3 and Pax7 function: implications for alveolar rhabdomyosarcoma cell of origin. Genes Develop. 18: 2608-2613.
42. Baudet, C. et al. 2008. Retrograde signaling onto Ret during motor nerve terminal maturation. J. Neurosci. 28: 963-975.
43. Hippenmeyer, S. et al. 2005. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3: e159.
44. Briscoe, J. et al. 1999. Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398: 622-627.
45. Zhang, Y. et al. 2008. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 60: 84-96.
46. Crone, S.A. et al. 2008. Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 60: 70-83.
47. Quinlan, K.A. & O. Kiehn . 2007. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J. Neurosci. 27: 6521-6530.
48. Burrill, J.D. et al. 1997. PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1 +interneurons that require PAX6 for their development. Development 124: 4493-4503.
49. Saueressig, H., J. Burrill & M. Goulding . 1999. Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126: 4201-4212.
50. Higashijima, S. et al. 2004. Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J. Neurosci. 24: 5827-5839.
51. Li, W.C. et al. 2004. Primitive roles for inhibitory interneurons in developing frog spinal cord. J. Neurosci. 24: 5840-5848.
52. Alvarez, F.J. et al. 2005. Postnatal phenotype and localization of spinal cord V1 derived interneurons. J. Comp. Neurol. 493: 177-192.
53. Sapir, T. et al. 2004. Pax6 and engrailed 1 regulate two distinct aspects of renshaw cell development. J. Neurosci. 24: 1255-1264.
54. Wenner, P., M.J. O'Donovan & M.P. Matise . 2000. Topographical and physiological characterization of interneurons that express engrailed-1 in the embryonic chick spinal cord. J. Neurophysiol. 84: 2651-2657.
55. Gosgnach, S. et al. 2006. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440: 215-219.
56. Karunaratne, A. et al. 2002. GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Develop. Biol. 249: 30-43.
57. Smith, E. et al. 2002. Coexpression of SCL and GATA3 in the V2 interneurons of the developing mouse spinal cord. Dev. Dyn. 224: 231-237.
58. Crone, S.A. et al. 2009. In mice lacking V2a interneurons, gait depends on speed of locomotion. J. Neurosci. 29: 7098-7109.
59. Dyck, J., G.M. Lanuza & S. Gosgnach . 2012. Functional characterization of dI6 interneurons in the neonatal mouse spinal cord. J. Neurophysiol. 107: 3256-3266.
60. Betley, J.N. et al. 2009. Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit. Cell 139: 161-174.
61. Stepien, A.E., M. Tripodi & S. Arber . 2010. Monosynaptic rabies virus reveals premotor network organization and synaptic specificity of cholinergic partition cells. Neuron 68: 456-472.
62. Bui, T.V. & R.M. Brownstone . 2010. dI3 neurons are rhythmically active during fictive locomotion. Presented at Society for Neuroscience, San Diego.
63. Enjin, A. et al. 2010. Identification of novel spinal cholinergic genetic subtypes disclose Chodl and Pitx2 as markers for fast motor neurons and partition cells. J. Comp. Neurol. 518: 2284-2304.
64. Zagoraiou, L. et al. 2009. A cluster of cholinergic premotor interneurons modulates mouse locomotor activity. Neuron 64: 645-662.
65. Hong, C.S., B.Y. Park & J.P. Saint-Jeannet . 2007. The function of Dmrt genes in vertebrate development: it is not just about sex. Dev. Biol. 310: 1-9.
66. Kim, S. et al. 2003. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Exp. Patterns 3: 77-82.
67. Andersson, L.S. et al. 2012. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice. Nature 488: 642-646.
68. Goulding, M. 2009. Circuits controlling vertebrate locomotion: moving in a new direction. Nature Rev. 10: 507-518.
69. Ahituv, N. et al. 2007. Deletion of ultraconserved elements yields viable mice. PLoS Biol. 5: e234.
70. Vallstedt, A. et al. 2001. Different levels of repressor activity assign redundant and specific roles to Nkx6 genes in motor neuron and interneuron specification. Neuron 31: 743-755.
71. Cowley, K.C. & B.J. Schmidt . 1995. Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J. Neurophysiol. 74: 1109-1117.
72. Jankowska, E. & B.R. Noga . 1990. Contralaterally projecting lamina VIII interneurones in middle lumbar segments in the cat. Brain Res. 535: 327-330.
73. Grillner, S. & P. Wallen . 1980. Does the central pattern generation for locomotion in lamprey depend on glycine inhibition? Acta Physiol. Scand. 110: 103-105.
74. Harris-Warrick, R.M. 2011. Neuromodulation and flexibility in Central Pattern Generator networks. Curr. Opin. Neurobiol. 21: 685-692.
75. McLean, D.L. et al. 2007. A topographic map of recruitment in spinal cord. Nature 446: 71-75.
76. Zhong, G., K. Sharma & R.M. Harris-Warrick . 2011. Frequency-dependent recruitment of V2a interneurons during fictive locomotion in the mouse spinal cord. Nat. Commun. 2: 274.
77. Grillner, S. 1975. Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol. Rev. 55: 247-304.
78. Ericson, J. et al. 1996. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87: 661-673.
79. Jostes, B., C. Walther & P. Gruss . 1990. The murine paired box gene, Pax7, is expressed specifically during the development of the nervous and muscular system. Mech. Dev. 33: 27-37.