Molecular gradients and development of retinotopic maps

Annual Review of Neuroscience

Volumn 28, Issue , 2005, Pages 327-355

  McLaughlin, Todd ^a   O'Leary, Dennis D M ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Axon branching; Axon guidance; Bidirectional signaling; Ephrins; Ephs; Visual system development

Indexed keywords

EPHRIN A1; EPHRIN B1; PROTEIN TYROSINE KINASE;

BRAIN MAPPING; MODEL; NERVE CELL NETWORK; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; VISUAL NERVOUS SYSTEM; VOMERONASAL ORGAN;

ANIMALS; AXONS; BRAIN MAPPING; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MODELS, BIOLOGICAL; RECEPTORS, EPH FAMILY; RETINA; RETINAL GANGLION CELLS; VISUAL PATHWAYS;

EID: 23244464284     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.neuro.28.061604.135714     Document Type: Review

References (142)

1. Alsina B, Vu T, Cohen-Cory S. 2001. Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat. Neurosci. 4:1093-101
2. Baier H, Bonhoeffer F. 1992. Axon guidance by gradients of a target-derived component. Science 255:472-75
3. Baier H, Klostermann S, Trowe T, Karlstrom RO, Nusslein-Volhard C, Bonhoeffer F. 1996. Genetic dissection of the retinotectal projection. Development 123:415-25
4. Bassell GJ, Kelic S. 2004. Binding proteins for mRNA localization and local translation, and their dysfunction in genetic neurological disease. Curr. Opin. Neurobiol. 14:574-81
5. Belluscio L, Koentges G, Axel R, Dulac C. 1999. A map of pheromone receptor activation in the mammalian brain. Cell 97:209-20
6. Benson DL, Colman DR, Huntley GW. 2001. Molecules, maps and synapse specificity. Nat. Rev. Neurosci. 2:899-909
7. Braisted JE, McLaughlin T, Wang HU, Friedman GC, Anderson DJ, O'Leary DDM. 1997. Graded and lamina-specific distributions of ligands of EphB receptor tyrosine kinases in the developing retinotectal system. Dev. Biol. 191:14-28
8. Brennan C, Monschau B, Lindberg R, Guthrie B, Drescher U, et al. 1997. Two Eph receptor tyrosine kinase ligands control axon growth and may be involved in the creation of the retinotectal map in the zebrafish. Development 124:655-64
9. Brittis PA, Lu Q, Flanagan JG. 2002. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110:223-35
10. Brown A, Yates PA, Burrola P, Ortuno D, Vaidya A, et al. 2000. Topographic mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling. Cell 102:77-88
11. Bruckner K, Pasquale EB, Klein R. 1997. Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science 275:1640-43
12. Butts DA. 2002. Retinal waves: implications for synaptic learning rules during development. Neuroscientist 8:243-53
13. Campbell DS, Holt CE. 2001. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-26
14. Campbell DS, Regan AG, Lopez JS, Tannahill D, Harris WA, Holt CE. 2001. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21:8538-47
15. Chalupa LM, Snider CJ. 1998. Topographic specificity in the retinocollicular projection of the developing ferret: an anterograde tracing study. J. Comp. Neurol. 392:35-47
16. Chalupa LM, Snider CJ, Kirby MA. 1996. Topographic organization in the retinocollicular pathway of the fetal cat demonstrated by retrograde labeling of ganglion cells. J. Comp. Neurol. 368:295-303
17. Cheng HJ, Flanagan JG. 1994. Identification and cloning of ELF-1, a developmentally expressed ligand for the Mek4 and Sek receptor tyrosine kinases. Cell 79:157-68
18. Cheng HJ, Nakamoto M, Bergemann AD, Flanagan JG. 1995. Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82:371-81
19. Choi O, O'Leary DDM. 2000. Potential roles for BDNF and TrkB in developing topographic retinotectal projections. Soc. Neurosci. Abstr. 26 (Abstr.)
20. Choi SB, Yates PA, O'Leary DDM. 1998. Localized BDNF application induces branch-like structures along retinal axons. Soc. Neurosci. Abstr. 24 (Abstr.)
21. Ciossek T, Monschau B, Kremoser C, Loschinger J, Lang S, et al. 1998. Eph receptor-ligand interactions are necessary for guidance of retinal ganglion cell axons in vitro. Eur. J. Neurosci. 10:1574-80
22. Cline HT. 1998. Topographic maps: developing roles of synaptic plasticity. Curr. Biol. 8:R836-39
23. Cloutier JF, Giger RJ, Koentges G, Dulac C, Kolodkin AL, Ginty DD. 2002. Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons. Neuron 33:877-92
24. Cloutier JF, Sahay A, Chang EC, Tessier-Lavigne M, Dulac C, et al. 2004. Differential requirements for semaphorin 3 F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections. J. Neurosci. 24:9087-96
25. Cohen-Cory S. 2002. The developing synapse: construction and modulation of synaptic structures and circuits. Science 298:770-76
26. Cohen-Cory S, Fraser SE. 1995. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378:192-96
27. Connor RJ, Menzel P, Pasquale EB. 1998. Expression and tyrosine phosphorylation of Eph receptors suggest multiple mechanisms in patterning of the visual system. Dev. Biol. 193:21-35
28. Cox EC, Muller B, Bonhoeffer F. 1990. Axonal guidance in the chick visual system: posterior tectal membranes induce collapse of growth cones from the temporal retina. Neuron 4:31-37
29. Davenport RW, Thies E, Cohen ML. 1999. Neuronal growth cone collapse triggers lateral extensions along trailing axons. Nat. Neurosci. 2:254-59
30. Davy A, Gale NW, Murray EW, Klinghoffer RA, Soriano P, et al. 1999. Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev. 13:3125-35
31. Davy A, Robbins SM. 2000. Ephrin-A5 modulates cell adhesion and morphology in an integrin-dependent manner. EMBO J. 19:5396-405
32. Debski EA, Cline HT. 2002. Activity-dependent mapping in the retinotectal projection. Curr. Opin. Neurobiol. 12:93-99
33. Demyanenko GP, Maness PF. 2003. The L1 cell adhesion molecule is essential for topographic mapping of retinal axons. J. Neurosci. 23:530-38
34. Diaz E, Yang YH, Ferreira T, Loh KC, Okazaki Y, et al. 2003. Analysis of gene expression in the developing mouse retina. Proc. Natl. Acad. Sci. USA 100:5491-96
35. Ding Y, Marotte LR. 1997. The initial stages of development of the retinocollicular projection in the wallaby (Macropus eugenii): distribution of ganglion cells in the retina and their axons in the superior colliculus. Anat. Embryol. 194:301-17
36. Drescher U, Kremoser C, Handwerker C, Loschinger J, Noda M, Bonhoeffer F. 1995. In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-70
37. Dufour A, Seibt J, Passante L, Depaepe V, Ciossek T, et al. 2003. Area specificity and topography of thalamocortical projections are controlled by ephrin/Eph genes. Neuron 39:453-65
38. Eberhart J, Barr J, O'Connell S, Flagg A, Swartz ME, et al. 2004. Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons. J. Neurosci. 24:1070-78
39. Ensslen-Craig SE, Brady-Kalnay SM. 2004. Receptor protein tyrosine phosphatases regulate neural development and axon guidance. Dev. Biol. 275:12-22
40. Feldheim DA, Kim YI, Bergemann AD, Frisen J, Barbacid M, Flanagan JG. 2000. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25:563-74
41. Feldheim DA, Nakamoto M, Osterfield M, Gale NW, DeChiara TM, et al. 2004. Loss-of-function analysis of EphA receptors in retinotectal mapping. J. Neurosci. 24:2542-50
42. Feng G, Laskowski MB, Feldheim DA, Wang H, Lewis R, et al. 2000. Roles for ephrins in positionally selective synaptogenesis between motor neurons and muscle fibers. Neuron 25:295-306
43. Frisen J, Yates PA, McLaughlin T, Friedman GC, O'Leary DDM, Barbacid M. 1998. Ephrin-A5 (AL-1/RAGS) is essential for proper retinal axon guidance and topographic mapping in the mammalian visual system. Neuron 20:235-43
44. Galli L, Maffei L. 1988. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science 242:90-91
45. Gallo G, Letourneau PC. 2004. Regulation of growth cone actin filaments by guidance cues. J. Neurobiol. 58:92-102
46. Gao PP, Zhang JH, Yokoyama M, Racey B, Dreyfus CF, et al. 1996. Regulation of topographic projection in the brain: Elf-1 in the hippocamposeptal system. Proc. Natl. Acad. Sci. USA 93:11161-66
47. Gierer A. 1983. Model for the retino-tectal projection. Proc. B. Soc. London B. Biol. Sci. 218:77-93
48. Gierer A. 1987. Directional cues for growing axons forming the retinotectal projection. Development 101:479-89
49. Goodhill GJ, Baier H. 1998. Axon guidance: stretching gradients to the limit. Neural Comput. 10:521-27
50. Hansen MJ, Dallai GE, Flanagan JG. 2004. Retinal axon response to ephrin-As shows a graded, concentration-dependent transition from growth promotion to inhibition. Neuron 42:717-30
51. Harris WA, Holt CE, Bonhoeffer F. 1987. Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. Development 101:123-33
52. Hebb DO. 1949. The Organization of Behavior: A Neuropsychological Theory. New York: Wiley
53. Henkemeyer M, Orioli D, Henderson JT, Saxton TM, Roder J, et al. 1996. Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86:35-46
54. Himanen J-P, Chumley MJ, Lackmann M, Li C, Barton WA, et al. 2004. Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci. 7:501-9
55. Himanen JP, Nikolov DB. 2003. Eph signaling: a structural view. Trends Neurosci. 26:46-51
56. Hindges R, McLaughlin T, Genoud N, Henkemeyer M, O'Leary DDM. 2002. EphB forward signaling controls directional branch extension and arborization required for dorsal ventral retinotopic mapping. Neuron 35:475-87
57. Holland SJ, Gale NW, Mbamalu G, Yancopoulos GD, Henkemeyer M, Pawson T. 1996. Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 383:722-25
58. Hornberger MR, Dutting D, Ciossek T, Yamada T, Handwerker C, et al. 1999. Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons. Neuron 22:731-42
59. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF. 2003. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu. Rev. Neurosci. 26: 509-63
60. Hutson LD, Chien CB. 2002. Wiring the zebrafish: axon guidance and synaptogenesis. Curr. Opin. Neurobiol. 12:87-92
61. Huynh-Do U, Stein E, Lane AA, Liu H, Cerretti DP, Daniel TO. 1999. Surface densities of ephrin-B1 determine EphB1-coupled activation of cell attachment through alphavbeta3 and alpha5beta1 integrins. EMBO J. 18:2165-73
62. Itoh K, Cheng L, Kamei Y, Fushiki S, Kamiguchi H, et al. 2004. Brain development in mice lacking L1-L1 homophilic adhesion. J. Cell Biol. 165:145-54
63. Johnson KG, McKinnell IW, Stoker AW, Holt CE. 2001. Receptor protein tyrosine phosphatases regulate retinal ganglion cell axon outgrowth in the developing Xenopus visual system. J. Neurobiol. 49:99-117
64. Kaas JH. 1997. Topographic maps are fundamental to sensory processing. Brain Res. Bull. 44: 107-12
65. Kaethner RJ, Stuermer CA. 1992. Dynamics of terminal arbor formation and target approach of retinotectal axons in living zebrafish embryos: a time-lapse study of single axons. J. Neurosci. 12:3257-71
66. Karlstrom RO, Trowe T, Bonhoeffer F. 1997. Genetic analysis of axon guidance and mapping in the zebrafish. Trends Neurosci. 20:3-8
67. Karlstrom RO, Trowe T, Klostermann S, Baier H, Brand M, et al. 1996. Zebrafish mutations affecting retinotectal axon pathfinding. Development 123:427-38
68. Knoll B, Drescher U. 2002. Ephrin-As as receptors in topographic projections. Trends Neurosci. 25:145-49
69. Knoll B, Schmidt H, Andrews W, Guthrie S, Pini A, et al. 2003. On the topographic targeting of basal vomeronasal axons through Slit-mediated chemorepulsion. Development 130:5073-82
70. Knoll B, Zarbalis K, Wurst W, Drescher U. 2001. A role for the EphA family in the topographic targeting of vomeronasal axons. Development 128:895-906
71. Kobayashi T, Nakamura H, Yasuda M. 1990. Disturbance of refinement of retinotectal projection in chick embryos by TTX and grayanotoxin. Dev. Brain Res. 57:29-35
72. Kong H, Boulter J, Weber JL, Lai C, Chao MV. 2001. An evolutionarily conserved transmembrane protein that is a novel downstream target of neurotrophin and ephrin receptors. J. Neurosci. 21:176-85
73. Liu Y, Berndt J, Su F, Tawarayama H, Shoji W, et al. 2004. Semaphorin3D guides retinal axons along the dorsoventral axis of the tectum. J. Neurosci. 24:310-18
74. Loconto J, Papes F, Chang E, Stowers L, Jones EP, et al. 2003. Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112:607-18
75. Mann F, Miranda E, Weinl C, Harmer E, Holt CE. 2003. B-type Eph receptors and ephrins induce growth cone collapse through distinct intracellular pathways. J. Neurobiol. 57:323-36
76. Mann F, Ray S, Harris WA, Holt CE. 2002. Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands. Neuron 35:461-73
77. Marcus RC, Gale NW, Morrison ME, Mason CA, Yancopoulos GD. 1996. Eph family receptors and their ligands distribute in opposing gradients in the developing mouse retina. Dev. Biol. 180:786-89
78. Marston DJ, Dickinson S, Nobes CD. 2003. Rac-dependent trans-endocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat. Cell Biol. 5:879-88
79. McLaughlin T, Hindges R, O'Leary DDM. 2003a. Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol. 13:57-69
80. McLaughlin T, Hindges R, Yates PA, O'Leary DDM. 2003b. Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal-ventral retinotopic mapping. Development 130:2407-18
81. McLaughlin T, Torborg CL, Feller MB, O'Leary DDM. 2003c. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40:1147-60
82. McLoon SC. 1991. A monoclonal antibody that distinguishes between temporal and nasal retinal axons. J. Neurosci. 11:1470-77
83. Meister M, Wong RO, Baylor DA, Shatz CJ. 1991. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939-43
84. Menzel P, Valencia F, Godement P, Dodelet VC, Pasquale EB. 2001. Ephrin-A6, a new ligand for EphA receptors in the developing visual system. Dev. Biol. 230:74-88
85. Monnier PP, Sierra A, Macchi P, Deitinghoff L, Andersen JS, et al. 2002. RGM is a repulsive guidance molecule for retinal axons. Nature 419:392-95
86. Monschau B, Kremoser C, Ohta K, Tanaka H, Kaneko T, et al. 1997. Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. EMBO J. 16:1258-67
87. Mui SH, Hindges R, O'Leary DD, Lemke G, Bertuzzi S. 2002. The homeodomain protein Vax2 patterns the dorsoventral and nasotemporal axes of the eye. Development 129:797-804
88. Muller BK, Jay DG, Bonhoeffer F. 1996. Chromophore-assisted laser inactivation of a repulsive axonal guidance molecule. Curr. Biol. 6:1497-502
89. Murai KK, Pasquale EB. 2003. 'Eph'ective signaling: forward, reverse and crosstalk. J. Cell Sci. 116:2823-32
90. Nakamoto M, Cheng HJ, Friedman GC, McLaughlin T, Hansen MJ, et al. 1996. Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo. Cell 86:755-66
91. Nakamoto T, Kain KH, Ginsberg MH. 2004. Neurobiology: new connections between integrins and axon guidance. Curr. Biol. 14:121-23
92. Nakamura H, O'Leary DDM. 1989. Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order. J. Neurosci. 9:3776-95
93. Neuhauss SC. 2003. Behavioral genetic approaches to visual system development and function in zebrafish. J. Neurobiol. 54:148-60
94. Neuhauss SC, Biehlmaier O, Seeliger MW, Das T, Kohler K, et al. 1999. Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. J. Neurosci. 19:8603-15
95. Nguyen QT, Sanes JR, Lichtman JW. 2002. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5:861-67
96. Niederkofler V, Salie R, Sigrist M, Arber S. 2004. Repulsive guidance molecule (RGM) gene function is required for neural tube closure but not retinal topography in the mouse visual system. J. Neurosci. 24:808-18
97. O'Leary DDM, Yates P, McLaughlin T. 1999. Mapping sights and smells in the brain: distinct mechanisms to achieve a common goal. Cell 96:255-69
98. O'Rourke NA, Cline HT, Fraser SE. 1994. Rapid remodeling of retinal arbors in the tectum with and without blockade of synaptic transmission. Neuron 12:921-34
99. O'Rourke NA, Fraser SE. 1990. Dynamic changes in optic fiber terminal arbors lead to retinotopic map formation: an in vivo confocal microscopic study. Neuron 5:159-71
100. Palmer A, Klein R. 2003. Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function. Genes Dev. 17:1429-50
101. Palmer A, Zimmer M, Erdmann KS, Eulenburg V, Porthin A, et al. 2002. EphrinB phosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase. Mol. Cell 9:725-37
102. Poliakov A, Cotrina M, Wilkinson DG. 2004. Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell 7:465-80
103. Prestige MC, Willshaw DJ. 1975. On a role for competition in the formation of patterned neural connexions. Proc. R. Soc. London B Biol. Sci. 190:77-98
104. Rajagopalan S, Deitinghoff L, Davis D, Conrad S, Skutella T, et al. 2004. Neogenin mediates the action of repulsive guidance molecule. Nat. Cell Biol. 6:756-62
105. Reber M, Burrola P, Lemke G. 2004. A relative signalling model for the formation of a topographic neural map. Nature 431:847-53
106. Rodriguez I, Feinstein P, Mombaerts P. 1999. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal system. Cell 97:199-208
107. Rosentreter SM, Davenport RW, Loschinger J, Huf J, Jung J, Bonhoeffer F. 1998. Response of retinal ganglion cell axons to striped linear gradients of repellent guidance molecules. J. Neurobiol. 37:541-62
108. Roskies A, Friedman G, O'Leary DDM. 1995. Molecules and mechanisms in the development of retinotopic maps. Perspect. Dev. Neurobiol. 3:63-75
109. Roskies AL, O'Leary DDM. 1994. Control of topographic retinal axon branching by inhibitory membrane-bound molecules. Science 265:799-803
110. Rosoff WJ, Urbach JS, Esrick MA, McAllister RG, Richards LJ, Goodhill GJ. 2004. A new chemotaxis assay shows the extreme sensitivity of axons to molecular gradients. Nat. Neurosci. 7:678-82
111. Rossant J, Hirashima M. 2003. Vascular development and patterning: making the right choices. Curr. Opin. Genet. Dev. 13:408-12
112. Ruthazer ES, Akerman CJ, Cline HT. 2003. Control of axon branch dynamics by correlated activity in vivo. Science 301:66-70
113. Sakurai T, Wong E, Drescher U, Tanaka H, Jay DG. 2002. Ephrin-A5 restricts topographically specific arborization in the chick retinotectal projection in vivo. Proc. Natl. Acad. Sci. USA 99:10795-800
114. Savitt JM, Trisler D, Hilt DC. 1995. Molecular cloning of TOP AP: a topographically graded protein in the developing chick visual system. Neuron 14:253-61
115. Schulte D, Furukawa T, Peters MA, Kozak CA, Cepko CL. 1999. Misexpression of the Emx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 24:541-53
116. Simon DK, O'Leary DDM. 1991. Relationship of retinotopic ordering of axons in the optic pathway to the formation of visual maps in central targets. J. Comp. Neurol. 307:393-404
117. Simon DK, O'Leary DDM. 1992a. Development of topographic order in the mammalian retinocollicular projection. J. Neurosci. 12:1212-32
118. Simon DK, O'Leary DDM. 1992b. Influence of position along the medial-lateral axis of the superior colliculus on the topographic targeting and survival of retinal axons. Dev. Brain Res. 69:167-72
119. Simon DK, O'Leary DDM. 1992c. Responses of retinal axons in vivo and in vitro to position-encoding molecules in the embryonic superior colliculus. Neuron 9:977-89
120. Simon DK, Prusky GT, O' Leary DDM, Constantine-Paton M. 1992. N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proc. Natl. Acad. Sci. USA 89:10593-97
121. Sperry R. 1963. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50:703-10
122. Stahl B, Muller B, von Boxberg Y, Cox EC, Bonhoeffer F. 1990. Biochemical characterization of a putative axonal guidance molecule of the chick visual system. Neuron 5:735-43
123. Stent GS. 1973. A physiological mechanism for Hebb's postulate of learning. Proc. Natl. Acad. Sci. USA 70:997-1001
124. Suh LH, Oster SF, Soehrman SS, Grenningloh G, Sretavan DW. 2004. L1/Laminin modulation of growth cone response to EphB triggers growth pauses and regulates the microtubule destabilizing protein SCG10. J. Neurosci. 24:1976-86
125. Surawska H, Ma PC, Salgia R. 2004. The role of ephrins and Eph receptors in cancer. Cytokine Growth Factor Rev. 15:419-33
126. Tian N, Copenhagen DR. 2003. Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39:85-96
127. Trowe T, Klostermann S, Baier H, Granato M, Crawford AD, et al. 1996. Mutations disrupting the ordering and topographic mapping of axons in the retinotectal projection of the zebrafish, Danio rerio. Development 123:439-50
128. van Horck FP, Weinl C, Holt CE. 2004. Retinal axon guidance: novel mechanisms for steering. Curr. Opin. Neurobiol. 14:61-66
129. Vanderhaeghen P, Polleux F. 2004. Developmental mechanisms patterning thalamocortical projections: intrinsic, extrinsic and in between. Trends Neurosci. 27:384-91
130. Wagle M, Grunewald B, Subburaju S, Barzaghi C, Le Guyader S, et al. 2004. EphrinB2a in the zebrafish retinotectal system. J. Neurobiol. 59:57-65
131. Walter J, Henke-Fahle S, Bonhoeffer F. 1987b. Avoidance of posterior tectal membranes by temporal retinal axons. Development 101:909-13
132. Walter J, Kern-Veits B, Huf J, Stolze B, Bonhoeffer F. 1987a. Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101:685-96
133. Walz A, Rodriguez I, Mombaerts P. 2002. Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. J. Neurosci. 22:4025-35
134. Weinl C, Drescher U, Lang S, Bonhoeffer F, Loschinger J. 2003. On the turning of Xenopus retinal axons induced by ephrin-A5. Development 130:1635-43
135. Wong EV, Kerner JA, Jay DG. 2004. Convergent and divergent signaling mechanisms of growth cone collapse by ephrinA5 and slit2. J. Neurobiol. 59:66-81
136. Wong RO, Meister M, Shatz CJ. 1993. Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11:923-38
137. Wong RO. 1999. Retinal waves and visual system development. Annu. Rev. Neurosci. 22:29-47
138. Yates PA, Holub AD, McLaughlin T, Sejnowski TJ, O'Leary DD. 2004. Computational modeling of retinotopic map development to define contributions of EphA-ephrinA gradients, axon-axon interactions, and patterned activity. J. Neurobiol. 59:95-113
139. Yates PA, Resides AR, McLaughlin T, O'Leary DDM. 2001. Topographic specific axon branching controlled by ephrin-As is the critical event in retinotectal map development. J. Neurosci. 21:8548-63
140. Yoda H, Hirose Y, Yasuoka A, Sasado T, Morinaga C, et al. 2004. Mutations affecting retinotectal axonal pathfinding in Medaka, Oryzias latipes. Mech. Dev. 121:715-28
141. Yue Y, Chen ZY, Gale NW, Blair-Flynn J, Hu TJ, et al. 2002. Mistargeting hippocampal axons by expression of a truncated Eph receptor. Proc. Natl. Acad. Sci. USA 99:10777-82
142. Zimmer M, Palmer A, Kohler J, Klein R. 2003. EphB-ephrinB bi-directional endocytosis terminates adhesion allowing contact mediated repulsion. Nat. Cell Biol. 5:869-78