Increasing the frequency of spontaneous rhythmic activity disrupts pool-specific axon fasciculation and pathfinding of embryonic spinal motoneurons

Journal of Neuroscience

Volumn 26, Issue 49, 2006, Pages 12769-12780

  Hanson, M Gartz ^a,b   Landmesser, Lynn T ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Axon guidance; Glycine; GlyT1 transporter; Motoneuron pool; Spinal cord; Spontaneous activity

Indexed keywords

SARCOSINE; STRYCHNINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; MUSCLE EXCITATION; NERVE CONDUCTION; NERVE FIBER; NERVE FUNCTION; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD MOTONEURON; SPINAL NERVE;

ACTION POTENTIALS; ANIMALS; AXONS; CHICK EMBRYO; GLYCINE; MOTOR NEURONS; NEURAL PATHWAYS; OVUM; SARCOSINE;

EID: 33845395809     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4170-06.2006     Document Type: Article

References (67)

1. Al-Majed AA, Brushart TM, Gordon T (2000) Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating femoral motoneurons. Eur J Neurosci 12:4381-4390.
2. Balcowiec A, Katz DM (2002) Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22:10339-10407.
3. Berghuis P, Dobszay MB, Sousa KM, Schulte G, Mager PP, Hartig W, Gores TJ, Zilberted Y, Ernfors P, Harkany T (2004) Brain-derived neurotrophic factor controls functional differentiation and microcircuit formation of selectively isolated fast-spiking GABAergic interneurons. Eur J Neurosci 20:1290-1306.
4. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC (2004) Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429:523-530.
5. Busetto G, Buffelli M, Tognana E, Bellico F, Cangiano A (2000) Hebbian mechanisms revealed by electrical stimulation at developing rat neuromuscular junctions. J Neurosci 20:685-695.
6. Cang J, Renteria RC, Kaneko M, Liu X, Copenhagen DR, Stryker MP (2005) Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 48:797-809.
7. Chandrasekaran AR, Plas DT, Gonzalez E, Crair MC (2005) Evidence for an instructive role of retinal activity in retinotopic map refinement in the superior colliculus of the mouse. J Neurosci 25:6929-6938.
8. Chang KT, Berg DK (2001) Voltage-gated channels block nicotinic regulation of CREB phosphorylation and gene expression in neurons. Neuron 32:855-865.
9. Chilton JK (2006) Molecular mechanisms of axon guidance. Dev Biol 292:13-24.
10. Cohen S, Funkelstein L, Livet J, Rougon G, Henderson CE, Castellani V, Mann F (2005) A semaphorin code defines subpopulations of spinal motor neurons during mouse development. Eur J Neurosci 21:1767-1776.
11. Dahm LM, Landmesser LT (1988) The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev Biol 130:621-644.
12. Dasen JS, Tice BC, Brenner-Morton S, Jessell TM (2005) A hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123:477-491.
13. Dickson BJ (2002) Molecular mechanisms of axon guidance. Science 298:1959-1964.
14. 2+ response amplitude and duration. Nature 386:855-858.
15. Eberhart J, Swartz ME, Koblar SA, Pasquale EB, Krull CE (2002) EphA4 constitutes a population-specific guidance cue for motor neurons. Dev Biol 247:89-101.
16. Eulenburg V, Armsen W, Betz H, Gomeza J (2005) Glycine transporters: essential regulators of neurotransmission. Trends Biochem Sci 30:325-333.
17. Goldinger A, Muller WE, Wollert U (1981) Inhibition of glycine and GABA receptor binding by several opiate agonists and antagonists. Gen Pharmacol 12:477-479.
18. Grubb MS, Rossi FM, Changeux JP, Thompson ID (2003) Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor. Neuron 40:1161-1172.
19. Hanson MG, Landmesser LT (2003) Characterization of the circuits that generate spontaneous episodes of activity in the early embryonic spinal cord. J Neurosci 23:587-600.
20. Hanson MG, Landmesser LT (2004) Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 46:687-701.
21. Hebb DO (1949) The organization of behavior. New York: Wiley.
22. Helmbacher F, Schneider-Maunoury S, Topilko P, Tiret L, Charney P (2000) Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 127:3313-3324.
23. Huber AB, Kania A, Tran TS, Gu C, De Marco Garcia N, Lieberam I, Johnson D, Jessell TM, Ginty DD, Kolodkin AL (2005) Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48:949-964.
24. Itoh K, Ozaki M, Stevens B, Fields RD (1997) Activity dependent regulation of N-cadherin in DRG neurons: differential regulation of N-cadherin, NCAM, and L1 by distinct patterns of action potentials. J Neurobiol 33:735-748.
25. Kania A, Jessell TM (2003) Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A: EphA interactions. Neuron 38:581-596.
26. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
27. Kim G, Kandler K (2003) Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6:282-290.
28. Kramer ER, Knott L, Su F, Dessaud E, Krull CE, Helmbacher F, Klein R (2006) Cooperation between GDNF/Ret and ephrinA/EphA4 signals for motor-axon pathway selection in the limb. Neuron 50:35-47.
29. 2+]I rise in fetal rat motoneurons in situ. J Neurosci 20:7905-7913.
30. Lance-Jones C, Landmesser L (1981a) Pathway selection by chick lumbosacral motoneurons during normal development. Proc R Soc Lond B Biol Sci 214:1-18.
31. Lance-Jones C, Landmesser LT (1981b) Pathway selection by embryonic chick lumbosacral motoneurons in an experimentally altered environment. Proc R Soc Lond B Biol Sci 214:19-52.
32. Landmesser LT (1978) The distribution of motoneurons supplying chick hind limb muscles. J Physiol (Lond) 284:371-389.
33. Landmesser LT, Morris DG (1975) The development of functional innervation in the hindlimb of the chick embryo. J Physiol (Lond) 249:301-326.
34. Landmesser LT, O'Donovan MJ (1984a) Activation patterns of embryonic chick hind limb muscles recorded in-ovo and in an isolated spinal cord preparation. J Physiol (Lond) 347:189-204.
35. Landmesser LT, O'Donovan MJ (1984b) The activation patterns of embryonic chick motoneurons projecting to inappropriate muscles. J Physiol (Lond) 347:205-224.
36. Li X, Gutierrez DV, Hanson MG, Han J, Mark MD, Chiel H, Hegemann P, Landmesser LT, Herlitze S (2005) Fast non-invasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channel rhodopsin. Proc Natl Acad Sci USA 102:17816-17821.
37. Lin JH, Saito T, Anderson DJ, Lance-Jones C, Jessell TM, Arber S (1998) Functionally related motor neuron pool and muscle sensory afferent subtypes defined by co-ordinate ETS gene expression. Cell 95:393-407.
38. Matise MP, Lance-Jones C (1996) A critical period for the specification of motor pools in the chick lumbosacral spinal cord. Development 122:659-669.
39. McLaughlin T, Torborg CL, Feller MB, O'Leary DD (2003) Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40:1147-1160.
40. Meyer-Franke A, Wilkinson GA, Kruttgen A, Hu K, Munro E, Hanson MG, Reichardt LF, Barres BA (1998) Depolarization and camp elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21:681-693.
41. Milner LD, Landmesser LT (1999) Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J Neurosci 19:3007-3022.
42. Moody WJ, Bosma MM (2004) Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev 85:883-941.
43. Nguyen L, Rigo J-M, Rocher V, Belachew S, Malgrange B, Rogister B, Leprince P, Moonen G (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res 305:187-202.
44. Nishimaru H, Iizuki S, Ozaki S, Kudo N (1996) Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J Physiol (Lond) 497:132-143.
45. O'Donovan MJ (1989) Motor activity in the isolated spinal cord of the chick embryo: synaptic drive and firing properties of single motoneurons. J Neurosci 9:943-958.
46. Owens DF, Kriegstein AR (2002) Developmental neurotransmitters? Neuron 36:989-995.
47. Penn AA, Riquelme PA, Feller MB, a Shatz CJ (1998) Competition in retinogeniculate patterning driven by spontaneous activity. Science 279:2108-2112.
48. Pittman RH, Oppenheim RW (1978) Neuromuscular blockade increases motoneurone survival during normal cell death in the embryo. Nature 271:425-446.
49. Rafuse VF, Milner L, Landmesser LT (1996) Selective innervation of fast and slow muscle regions during early chick neuromuscular development. J Neurosci 16:6864-6877.
50. Ren J, Greer JJ (2003) Ontogeny of rhythmic motor patterns in the embryonic rat spinal cord. J Neurophysiol 89:1187-1195.
51. Rossi FM, Pizzorusso T, Porciatti V, Marubio LM, Maffei L, Changeux JP (2001) requirement of the nicotinic acetylcholine receptor β2 subunit for the anatomical and functional development of the visual system. Proc Natl Acad Sci USA 98:6453-6458.
52. Ruthazer ES, Li J, Cline HT (2006) Stabilization of axon branch dynamics by synaptic maturation. J Neurosci 26:3594-3603.
53. Sengpiel F, Kind PC (2002) The role of activity in development of the visual system. Curr Biol 12:R18-R26.
54. Shah V, Drill E, Lance-Jones C (2004) Ectopic expression of Hoxd10 in thoracic spinal segments induces motoenurons with lumbosacral molecular profile and axon projections to limb. Dev Dyn 231:43-56.
55. Shirasaki R, Lewcock JW, Lettieri K, Pfaff SL (2006) FGF as a target derived chemoattractant for developing motor axons genetically programmed by the LIM code. Neuron 50:841-853.
56. Stellwagen D, Shatz CJ (2002) An instructive role for retinal waves in the development of retinogenicuate connectivity. Neuron 33:357-367.
57. Tang J, Landmesser L, Rutishahuser U (1992) Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 8:1031-1044.
58. Tang J, Rutishauser U, Landmesser L (1994) Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 13:405-414.
59. Tao HW, Poo M-m (2005) Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45:829-836.
60. Thompson WJ (1983) Synapse elimination in neonatal rat muscle is sensitive to the apttern of muscle use. Nature 302:614-616.
61. Torborg CL, Feller MB (2005) Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol 76:213-235.
62. Torborg CL, Hansen KA, Feller MB (2005) High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat Neurosci 8:72-78.
63. Watt SD, Gu X, Smith RD, Spitzer NC (2000) Specific frequencies of spontaneous Ca2+ transients upregulate GAD 67 transcripts in embryonic spinal neurons. Mol Cell Neurosci 16:376-387.
64. Wu GY, Deisseroth K, Tsien RW (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci 4:151-158.
65. Wu W, Ziskind-Conhaim L, Sweet MA (1992) Early development of glycine- and GABA-mediated synapses in rat spinal cord. J Neurosci 12:3935-3945.
66. Young AB, Snyder SH (1973) Strychnine binding associated with glycine receptors of the central nervous system. Proc Natl Acad Sci USA 70:2832-2836.
67. Zhang, Tao HW, Holt CE, Harris WA, Poo M (1998) A critical window for cooperation and competition among developing retinotectal synapses. Nature 395:37-44.