Electrical activity as a developmental regulator in the formation of spinal cord circuits

Current Opinion in Neurobiology

Volumn 22, Issue 4, 2012, Pages 624-630

  Borodinsky, Laura N ^a   Belgacem, Yesser Hadj ^a   Swapna, Immani ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CALCIUM ION; NETRIN 1; SODIUM CHANNEL NAV1.6; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

CALCIUM SIGNALING; CELL COUNT; CELL CYCLE PROGRESSION; CELL FATE; CELL TYPE; GABAERGIC SYSTEM; HUMAN; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPINAL CORD DEVELOPMENT; SPINAL CORD FUNCTION; SPINAL CORD NERVE CELL; SPINAL CORD POTENTIAL; SYNAPTIC POTENTIAL; SYNAPTOGENESIS;

ANIMALS; HUMANS; LOCOMOTION; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; SPINAL CORD;

EID: 84865964551     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2012.02.004     Document Type: Review

References (57)

1. Tanabe Y., Jessell T.M. Diversity and pattern in the developing spinal cord. Science 1996, 274:1115-1123.
2. Alvarez F.J., Jonas P.C., Sapir T., Hartley R., Berrocal M.C., Geiman E.J., Todd A.J., Goulding M. Postnatal phenotype and localization of spinal cord V1 derived interneurons. J Comp Neurol 2005, 493:177-192.
3. Song M.R., Sun Y., Bryson A., Gill G.N., Evans S.M., Pfaff S.L. Islet-to-LMO stoichiometries control the function of transcription complexes that specify motor neuron and V2a interneuron identity. Development 2009, 136:2923-2932.
4. McDearmid J.R., Liao M., Drapeau P. Glycine receptors regulate interneuron differentiation during spinal network development. Proc Natl Acad Sci U S A 2006, 103:9679-9684.
5. Reynolds A., Brustein E., Liao M., Mercado A., Babilonia E., Mount D.B., Drapeau P. Neurogenic role of the depolarizing chloride gradient revealed by global overexpression of KCC2 from the onset of development. J Neurosci 2008, 28:1588-1597.
6. Banks G.B., Kanjhan R., Wiese S., Kneussel M., Wong L.M., O'Sullivan G., Sendtner M., Bellingham M.C., Betz H., Noakes P.G. Glycinergic and GABAergic synaptic activity differentially regulate motoneuron survival and skeletal muscle innervation. J Neurosci 2005, 25:1249-1259.
7. Oppenheim R.W., Caldero J., Cuitat D., Esquerda J., Ayala V., Prevette D., Wang S. Rescue of developing spinal motoneurons from programmed cell death by the GABA(A) agonist muscimol acts by blockade of neuromuscular activity and increased intramuscular nerve branching. Mol Cell Neurosci 2003, 22:331-343.
8. Oppenheim R.W., Prevette D., Yin Q.W., Collins F., MacDonald J. Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 1991, 251:1616-1618.
9. Gould T.W., Enomoto H. Neurotrophic modulation of motor neuron development. Neuroscientist 2009, 15:105-116.
10. Svoboda K.R., Linares A.E., Ribera A.B. Activity regulates programmed cell death of zebrafish Rohon-Beard neurons. Development 2001, 128:3511-3520.
11. Hanson M.G., Landmesser L.T. Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 2004, 43:687-701.
12. Li H., de Faria J.P., Andrew P., Nitarska J., Richardson W.D. Phosphorylation regulates OLIG2 cofactor choice and the motor neuron-oligodendrocyte fate switch. Neuron 2011, 69:918-929.
13. Tripodi M., Stepien A.E., Arber S. Motor antagonism exposed by spatial segregation and timing of neurogenesis. Nature 2011, 479:61-66.
14. Borodinsky L.N., Root C.M., Cronin J.A., Sann S.B., Gu X., Spitzer N.C. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 2004, 429:523-530.
15. Marek K.W., Kurtz L.M., Spitzer N.C. cJun integrates calcium activity and tlx3 expression to regulate neurotransmitter specification. Nat Neurosci 2010, 13:944-950.
16. Belgacem Y.H., Borodinsky L.N. Sonic hedgehog signaling is decoded by calcium spike activity in the developing spinal cord. Proc Natl Acad Sci U S A 2011, 108:4482-4487.
17. Tallafuss A., Eisen J.S. The Met receptor tyrosine kinase prevents zebrafish primary motoneurons from expressing an incorrect neurotransmitter. Neural Dev 2008, 3:18.
18. Hale L.A., Fowler D.K., Eisen J.S. Netrin signaling breaks the equivalence between two identified zebrafish motoneurons revealing a new role of intermediate targets. PLoS One 2011, 6:e25841.
19. Bradley S., Tossell K., Lockley R., McDearmid J.R. Nitric oxide synthase regulates morphogenesis of zebrafish spinal cord motoneurons. J Neurosci 2010, 30:16818-16831.
20. Prithviraj R., Kelly K.M., Espinoza-Lewis R., Hexom T., Clark A.B., Inglis F.M. Differential regulation of dendrite complexity by AMPA receptor subunits GluR1 and GluR2 in motor neurons. Dev Neurobiol 2008, 68:247-264.
21. Inglis F.M., Crockett R., Korada S., Abraham W.C., Hollmann M., Kalb R.G. The AMPA receptor subunit GluR1 regulates dendritic architecture of motor neurons. J Neurosci 2002, 22:8042-8051.
22. Inglis F.M., Zuckerman K.E., Kalb R.G. Experience-dependent development of spinal motor neurons. Neuron 2000, 26:299-305.
23. Inglis F.M., Furia F., Zuckerman K.E., Strittmatter S.M., Kalb R.G. The role of nitric oxide and NMDA receptors in the development of motor neuron dendrites. J Neurosci 1998, 18:10493-10501.
24. Zhang L., Schessl J., Werner M., Bonnemann C., Xiong G., Mojsilovic-Petrovic J., Zhou W., Cohen A., Seeburg P., Misawa H., et al. Role of GluR1 in activity-dependent motor system development. J Neurosci 2008, 28:9953-9968.
25. Nishiyama M., Togashi K., von Schimmelmann M.J., Lim C.S., Maeda S., Yamashita N., Goshima Y., Ishii S., Hong K. Semaphorin 3A induces CaV2.3 channel-dependent conversion of axons to dendrites. Nat Cell Biol 2011, 13:676-685.
26. Hanson M.G., Landmesser L.T. Increasing the frequency of spontaneous rhythmic activity disrupts pool-specific axon fasciculation and pathfinding of embryonic spinal motoneurons. J Neurosci 2006, 26:12769-12780.
27. Kastanenka K.V., Landmesser L.T. In vivo activation of channelrhodopsin-2 reveals that normal patterns of spontaneous activity are required for motoneuron guidance and maintenance of guidance molecules. J Neurosci 2010, 30:10575-10585.
28. Dasen J.S., Jessell T.M. Hox networks and the origins of motor neuron diversity. Curr Top Dev Biol 2009, 88:169-200.
29. + channels affects zebrafish motoneuron development. Development 2006, 133:3827-3836.
30. Saint-Amant L., Drapeau P. Synchronization of an embryonic network of identified spinal interneurons solely by electrical coupling. Neuron 2001, 31:1035-1046.
31. Saint-Amant L., Drapeau P. Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. J Neurosci 2000, 20:3964-3972.
32. Personius K.E., Karnes J.L., Parker S.D. NMDA receptor blockade maintains correlated motor neuron firing and delays synapse competition at developing neuromuscular junctions. J Neurosci 2008, 28:8983-8992.
33. Gonzalez-Islas C., Wenner P. Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron 2006, 49:563-575.
34. Wilhelm J.C., Rich M.M., Wenner P. Compensatory changes in cellular excitability, not synaptic scaling, contribute to homeostatic recovery of embryonic network activity. Proc Natl Acad Sci U S A 2009, 106:6760-6765.
35. Fetcho J.R., McLean D.L. Some principles of organization of spinal neurons underlying locomotion in zebrafish and their implications. Ann N Y Acad Sci 2010, 1198:94-104.
36. McLean D.L., Fetcho J.R. Spinal interneurons differentiate sequentially from those driving the fastest swimming movements in larval zebrafish to those driving the slowest ones. J Neurosci 2009, 29:13566-13577.
37. McLean D.L., Fan J., Higashijima S., Hale M.E., Fetcho J.R. A topographic map of recruitment in spinal cord. Nature 2007, 446:71-75.
38. Pineda R.H., Ribera A.B. Dorsal-ventral gradient for neuronal plasticity in the embryonic spinal cord. J Neurosci 2008, 28:3824-3834.
39. Provine R.R., Sharma S.C., Sandel T.T., Hamburger V. Electrical activity in the spinal cord of the chick embryo, in situ. Proc Natl Acad Sci U S A 1970, 65:508-515.
40. Li J., Walker S.M., Fitzgerald M., Baccei M.L. Activity-dependent modulation of glutamatergic signaling in the developing rat dorsal horn by early tissue injury. J Neurophysiol 2009, 102:2208-2219.
41. Mercer A.R., Hildebrand J.G. Developmental changes in the electrophysiological properties and response characteristics of Manduca antennal-lobe neurons. J Neurophysiol 2002, 87:2650-2663.
42. Jiang S.A., Campusano J.M., Su H., O'Dowd D.K. Drosophila mushroom body Kenyon cells generate spontaneous calcium transients mediated by PLTX-sensitive calcium channels. J Neurophysiol 2005, 94:491-500.
43. Blanton M.G., Lo Turco J.J., Kriegstein A.R. Endogenous neurotransmitter activates N-methyl-d-aspartate receptors on differentiating neurons in embryonic cortex. Proc Natl Acad Sci U S A 1990, 87:8027-8030.
44. Demarque M., Spitzer N.C. Activity-dependent expression of Lmx1b regulates specification of serotonergic neurons modulating swimming behavior. Neuron 2010, 67:321-334.
45. Dulcis D., Spitzer N.C. Illumination controls differentiation of dopamine neurons regulating behaviour. Nature 2008, 456:195-201.
46. 2+ sources and effects of altered activation of transmitter receptors. J Neurosci 2009, 29:15232-15244.
47. O'Donovan M.J., Wenner P., Chub N., Tabak J., Rinzel J. Mechanisms of spontaneous activity in the developing spinal cord and their relevance to locomotion. Ann N Y Acad Sci 1998, 860:130-141.
48. Feller M.B., Wellis D.P., Stellwagen D., Werblin F.S., Shatz C.J. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 1996, 272:1182-1187.
49. Wong R.O., Meister M., Shatz C.J. Transient period of correlated bursting activity during development of the mammalian retina. Neuron 1993, 11:923-938.
50. Singer J.H., Mirotznik R.R., Feller M.B. Potentiation of L-type calcium channels reveals nonsynaptic mechanisms that correlate spontaneous activity in the developing mammalian retina. J Neurosci 2001, 21:8514-8522.
51. Bansal A., Singer J.H., Hwang B.J., Xu W., Beaudet A., Feller M.B. Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. J Neurosci 2000, 20:7672-7681.
52. Torborg C.L., Hansen K.A., Feller M.B. High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat Neurosci 2005, 8:72-78.
53. McLaughlin T., Torborg C.L., Feller M.B., O'Leary D.D. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 2003, 40:1147-1160.
54. Penn A.A., Riquelme P.A., Feller M.B., Shatz C.J. Competition in retinogeniculate patterning driven by spontaneous activity. Science 1998, 279:2108-2112.
55. Cancedda L., Fiumelli H., Chen K., Poo M.M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 2007, 27:5224-5235.
56. Wang C.L., Zhang L., Zhou Y., Zhou J., Yang X.J., Duan S.M., Xiong Z.Q., Ding Y.Q. Activity-dependent development of callosal projections in the somatosensory cortex. J Neurosci 2007, 27:11334-11342.
57. De Marco Garcia N.V., Karayannis T., Fishell G. Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 2011, 472:351-355.