Failure to Maintain Eye-Specific Segregation in nob, a Mutant with Abnormally Patterned Retinal Activity

Neuron

Volumn 50, Issue 2, 2006, Pages 247-259

  Demas, Jay ^a   Sagdullaev, Botir T ^b   Green, Erick ^c   Jaubert Miazza, Lisa ^c   McCall, Maureen A ^b   Gregg, Ronald G ^b   Wong, Rachel O L ^a   Guido, William ^c  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DEVBIO; MOLNEURO; SYSNEURO

Indexed keywords

MUTANT PROTEIN; NYCTALOPIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EVOKED VISUAL RESPONSE; INTERNEURON; LATERAL GENICULATE NUCLEUS; MOUSE; MOUSE STRAIN; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REARING; RETINA; VISUAL SYSTEM;

ANIMALS; BODY PATTERNING; BRAIN MAPPING; GENICULATE BODIES; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MUTATION; PROTEOGLYCANS; RETINA; RETINAL GANGLION CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VISUAL PATHWAYS;

EID: 33646070275     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.03.033     Document Type: Article

References (63)

1. Akerman C.J., Smyth D., and Thompson I.D. Visual experience before eye-opening and the development of the retinogeniculate pathway. Neuron 36 (2002) 869-879
2. Akerman C.J., Grubb M.S., and Thompson I.D. Spatial and temporal properties of visual responses in the thalamus of the developing ferret. J. Neurosci. 24 (2004) 170-182
3. Allen L.E., Zito I., Bradshaw K., Patel R.J., Bird A.C., Fitzke F., Yates J.R., Trump D., Hardcastle A.J., and Moore A.T. Genotype-phenotype correlation in British families with X linked congenital stationary night blindness. Br. J. Ophthalmol. 87 (2003) 1413-1420
4. Ball S.L., Pardue M.T., McCall M.A., Gregg R.G., and Peachey N.S. Immunohistochemical analysis of the outer plexiform layer in the nob mouse shows no abnormalities. Vis. Neurosci. 20 (2003) 267-272
5. Bansal A., Singer J.H., Hwang B.J., Xu W., Beaudet A., and 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. 20 (2000) 7672-7681
6. Bech-Hansen N.T., Naylor M.J., Maybaum T.A., Sparkes R.L., Koop B., Birch D.G., Bergen A.A., Prinsen C.F., Polomeno R.C., Gal A., et al. Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat. Genet. 26 (2000) 319-323
7. Candille S.I., Pardue M.T., McCall M.A., Peachey N.S., and Gregg R.G. Localization of the mouse nob (no b-wave) gene to the centromeric region of the X chromosome. Invest. Ophthalmol. Vis. Sci. 40 (1999) 2748-2751
8. Chapman B. Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science 287 (2000) 2479-2482
9. Chen C., and Regehr W.G. Developmental remodeling of the retinogeniculate synapse. Neuron 28 (2000) 955-966
10. Cook P.M., Prusky G., and Ramoa A.S. The role of spontaneous retinal activity before eye opening in the maturation of form and function in the retinogeniculate pathway of the ferret. Vis. Neurosci. 16 (1999) 491-501
11. Demas J., Eglen S.J., and Wong R.O. Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience. J. Neurosci. 23 (2003) 2851-2860
12. Dubin M.W., Stark L.A., and Archer S.M. A role for action-potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. J. Neurosci. 6 (1986) 1021-1036
13. Eglen S.J. The role of retinal waves and synaptic normalization in retinogeniculate development. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354 (1999) 497-506
14. Enz R., Brandstatter J.H., Hartveit E., Wassle H., and Bormann J. Expression of GABA receptor rho 1 and rho 2 subunits in the retina and brain of the rat. Eur. J. Neurosci. 7 (1995) 1495-1501
15. Enz R., Brandstatter J.H., Wassle H., and Bormann J. Immunocytochemical localization of the GABAc receptor rho subunits in the mammalian retina. J. Neurosci. 16 (1996) 4479-4490
16. Feller M.B., Wellis D.P., Stellwagen D., Werblin F.S., and Shatz C.J. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272 (1996) 1182-1187
17. Garaschuk O., Hanse E., and Konnerth A. Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J. Physiol. 507 (1998) 219-236
18. Godement P., Salaun J., and Imbert M. Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J. Comp. Neurol. 230 (1984) 552-575
19. Goldberg J.L., Espinosa J.S., Xu Y., Davidson N., Kovacs G.T., and Barres B.A. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33 (2002) 689-702
20. Gregg R.G., Mukhopadhyay S., Candille S.I., Ball S.L., Pardue M.T., McCall M.A., and Peachey N.S. Identification of the gene and the mutation responsible for the mouse nob phenotype. Invest. Ophthalmol. Vis. Sci. 44 (2003) 378-384
21. Gregg, R.G., McCall, M.A., and Peachey, N.S. (2005). Bipolar specific expression of nyctalopin fusion gene rescues No-B wave phenotype in Nob mice. ARVO Abstracts.
22. Grubb M.S., Rossi F.M., Changeux J.P., and Thompson I.D. Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor. Neuron 40 (2003) 1161-1172
23. Hua J.Y., Smear M.C., Baier H., and Smith S.J. Regulation of axon growth in vivo by activity-based competition. Nature 434 (2005) 1022-1026
24. Hubel D.H. Tungsten microelectrode for recording from single units. Science 125 (1957) 549-550
25. Huberman A.D., Wang G.Y., Liets L.C., Collins O.A., Chapman B., and Chalupa L.M. Eye-specific retinogeniculate segregation independent of normal neuronal activity. Science 300 (2003) 994-998
26. Huberman A.D., Murray K.D., Warland D.K., Feldheim D.A., and Chapman B. Ephrin-As mediate targeting of eye-specific projections to the lateral geniculate nucleus. Nat. Neurosci. 8 (2005) 1013-1021
27. Ihaka R., and Gentleman R. R: A Language for Data Analysis and Graphics. Journal of Graphical and Computational Statistics 5 (1996) 491-508
28. Jaubert-Miazza L., Green E., Lo F., Bui K., Mills J., and Guido W. Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis. Neurosci. 22 (2005) 661-676
29. Katz L.C., and Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 274 (1996) 1133-1138
30. Khan N.W., Kondo M., Hiriyanna K.T., Jamison J.A., Bush R.A., and Sieving P.A. Primate Retinal Signaling Pathways: Suppressing ON-Pathway Activity in Monkey With Glutamate Analogues Mimics Human CSNB1-NYX Genetic Night Blindness. J. Neurophysiol. 93 (2005) 481-492
31. Lee C.W., Eglen S.J., and Wong R.O. Segregation of ON and OFF retinogeniculate connectivity directed by patterned spontaneous activity. J. Neurophysiol. 88 (2002) 2311-2321
32. McLaughlin T., Torborg C.L., Feller M.B., and O'Leary D.D. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40 (2003) 1147-1160
33. Meister M., Wong R.O., Baylor D.A., and Shatz C.J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252 (1991) 939-943
34. Miyake Y., Yagasaki K., Horiguchi M., and Kawase Y. On- and off-responses in photopic electroretinogram in complete and incomplete types of congenital stationary night blindness. Jpn. J. Ophthalmol. 31 (1987) 81-87
35. Muir-Robinson G., Hwang B.J., and Feller M.B. Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J. Neurosci. 22 (2002) 5259-5264
36. O'Donovan M.J., and Landmesser L. The development of hindlimb motor activity studied in the isolated spinal cord of the chick embryo. J. Neurosci. 7 (1987) 3256-3264
37. Olney J.W. Centripetal sequence of appearance of receptor-bipolar synaptic structures in developing mouse retina. Nature 218 (1968) 281-282
38. Pardue M.T., McCall M.A., LaVail M.M., Gregg R.G., and Peachey N.S. A naturally occurring mouse model of X-linked congenital stationary night blindness. Invest. Ophthalmol. Vis. Sci. 39 (1998) 2443-2449
39. Personius K.E., and Balice-Gordon R.J. Loss of correlated motor neuron activity during synaptic competition at developing neuromuscular synapses. Neuron 31 (2001) 395-408
40. Pesch K., Zeitz C., Fries J.E., Munscher S., Pusch C.M., Kohler K., Berger W., and Wissinger B. Isolation of the mouse nyctalopin gene nyx and expression studies in mouse and rat retina. Invest. Ophthalmol. Vis. Sci. 44 (2003) 2260-2266
41. Pfeiffenberger C., Cutforth T., Woods G., Yamada J., Renteria R.C., Copenhagen D.R., Flanagan J.G., and Feldheim D.A. Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping. Nat. Neurosci. 8 (2005) 1022-1027
42. Pusch C.M., Zeitz C., Brandau O., Pesch K., Achatz H., Feil S., Scharfe C., Maurer J., Jacobi F.K., Pinckers A., et al. The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nat. Genet. 26 (2000) 324-327
43. Rossi F.M., Pizzorusso T., Porciatti V., Marubio L.M., Maffei L., and Changeux J.P. Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system. Proc. Natl. Acad. Sci. USA 98 (2001) 6453-6458
44. Ruthazer E.S., and Cline H.T. Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective. J. Neurobiol. 59 (2004) 134-146
45. Scholl H.P., Langrova H., Pusch C.M., Wissinger B., Zrenner E., and Apfelstedt-Sylla E. Slow and fast rod ERG pathways in patients with X-linked complete stationary night blindness carrying mutations in the NYX gene. Invest. Ophthalmol. Vis. Sci. 42 (2001) 2728-2736
46. Sernagor E., Eglen S.J., and O'Donovan M.J. Differential effects of acetylcholine and glutamate blockade on the spatiotemporal dynamics of retinal waves. J. Neurosci. 20 (2000) RC56
47. Shatz C.J. Emergence of order in visual system development. Proc. Natl. Acad. Sci. USA 93 (1996) 602-608
48. Stellwagen D., and Shatz C.J. An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33 (2002) 357-367
49. Stoica P., and Moses R.L. Introduction to Spectral Analysis (1997), Prentice Hall, Upper Saddle River, NJ
50. Tagawa Y., Sawai H., Ueda Y., Tauchi M., and Nakanishi S. Immunohistological studies of metabotropic glutamate receptor subtype 6-deficient mice show no abnormality of retinal cell organization and ganglion cell maturation. J. Neurosci. 19 (1999) 2568-2579
51. Tian N., and Copenhagen D.R. Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39 (2003) 85-96
52. Torborg C.L., and Feller M.B. Unbiased analysis of bulk axonal segregation patterns. J. Neurosci. Methods 135 (2004) 17-26
53. Torborg C.L., Hansen K.A., and Feller M.B. High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nat. Neurosci. 8 (2005) 72-78
54. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287 (2000) 864-869
55. Wiesel T.N. Postnatal development of the visual cortex and the influence of environment. Nature 299 (1982) 583-591
56. Willshaw D.J., and von der Malsburg C. How patterned neural connections can be set up by self-organization. Proc. R. Soc. Lond. B. Biol. Sci. 194 (1976) 431-445
57. Wong R.O. Retinal waves and visual system development. Annu. Rev. Neurosci. 22 (1999) 29-47
58. Wong R.O., and Oakley D.M. Changing patterns of spontaneous bursting activity of on and off retinal ganglion cells during development. Neuron 16 (1996) 1087-1095
59. Wong R.O., Meister M., and Shatz C.J. Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11 (1993) 923-938
60. Wong W.T., Sanes J.R., and Wong R.O. Developmentally regulated spontaneous activity in the embryonic chick retina. J. Neurosci. 18 (1998) 8839-8852
61. Young R.S.L. Low-frequency component of the photopic erg in patients with x-linked congenital stationary night blindness. Clin. Vis. Sci. 6 (1991) 309-315
62. Zhang L.I., and Poo M.M. Electrical activity and development of neural circuits. Nat. Neurosci. 4 Suppl. (2001) 1207-1214
63. Zhou Q., Tao H.W., and Poo M.M. Reversal and stabilization of synaptic modifications in a developing visual system. Science 300 (2003) 1953-1957