Abstract
The retino-tectal system has served as a model for the growth and navigation of axons in the developing brain for over 50 years, when the first anatomical studies of embryos revealed details of the ontogeny of this pathway (Herrick 1941). Such observations led to various enthusiastic speculations concerning axon growth, including ideas that growth cones were towed to their targets, or directed there by electric fields. These hypotheses were succeeded by others, slightly less fantastic, which had retinal axons following emerging cracks and channels in the brain that blazed the trail for their long journey (reviewed in Jacobson, 1991). In the 1960s, Sperry made what at first seemed like an equally wild hypothesis, that retinal axons were led to their specific targets in the tectum by cytochemical tags (Sperry 1963). For more than 30 years, Sperry’s hypothesis gained force as attempts to disprove or replace it with less biochemical hypotheses failed. Though success in the search for the molecular basis of retinal axon navigation, and the vindication of Sperry, had to wait until the 1990s and the second coming of age of molecular biology, the attraction of the retino-tectal system for investigating these fundamental issues has never diminished. As a result, this is one of the most carefully studied and well-characterized developing axon pathways known.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Baier H, Klostermann S, Trowe T, Karlstrom RO, Nusslein-Volhard C, Bonhoeffer F (1996) Genetic dissection of the retinotectal projection. Development 123: 415–425
Benowitz LI, Routtenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20: 84–91
Boncinelli E (1994) Early CNS development: distal-less related genes and forebrain development. Curr Opin Neurobiol 4: 29–36
Bonhoeffer F, Huf J (1985) Position-dependent properties of retinal axons and their growth cones. Nature 315: 409–410
Braisted JE, McLaughlin T, Wang HU, Friedman GC, Anderson DJ, O’Leary DD (1997) Graded and lamina-specific distributions of ligands of EphB receptor tyrosine kinases in the developing retinotectal system. Dev Biol 191: 14–28
Brittis PA, Lemmon V, Rutishauser U, Silver J (1995) Unique changes of ganglion cell growth cone behavior following cell adhesion molecule perturbations: a time-lapse study of the living retina. Mol Cell Neurosci 6: 433–449
Brittis PA, Silver J (1995) Multiple factors govern intraretinal axon guidance: a time-lapse study. Mol Cell Neurosci 6: 413–432
Brittis PA, Silver J, Walsh FS, Doherty P (1996) Fibroblast growth factor receptor function is required for the orderly projection of ganglion cell axons in the developing mammalian retina. Mol Cell Neurosci 8: 120–128
Chan SO, Baker GE, Guillery RW (1993) Differential action of the albino mutation on two components of the rat’s uncrossed retinofugal pathway. J Comp Neurol 336: 362–377
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: 371–381
Chien CB, Cornel EM, Holt CE (1995) Absence of topography in precociously innervated tecta. Development 121: 2621–2631
Chien CB, Rosenthal DE, Harris WA, Holt CE (1993) Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron 11: 237–251
Cima C, Grant P (1982) Development of the optic nerve in Xenopus laevis. I. Early development and organization. J Embryol Exp Morphol 72: 225–249
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: 2135
Cornel E, Holt C (1992) Precocious pathfinding: retinal axons can navigate in an axonless brain. Neuron 9: 1001–1011
Crossley PH, Martinez S, Martin GR (1996) Midbrain development induced by FGF8 in the chick embryo. Nature 380: 66–68
Deiner MS, Kennedy TE, Fazeli A, Serafini T, Tessier-Lavigne M, Sretavan DW (1997) Netrin-1 and DCC mediate axon guidance locally at the optic disk: loss of function leads to optic nerve hypoplasia. Neuron 19: 575–589
Doherty P, Walsh FS (1996) CAM-FGF receptor interactions: a model for axonal growth. Mol Cell Neurosci 8:99–111
Easter SS Jr, Bratton B, Scherer SS (1984) Growth-related order of the retinal fiber layer in goldfish. J Neurosci 4:2173–2190
Fawcett JW, Gaze RM (1982) The retinotectal fibre pathways from normal and compound eyes in Xenopus. J Embryol Exp Morphol 72: 19–37
Fawcett JW, Taylor JS, Gaze RM, Grant P, Hirst E (1984) Fibre order in the normal Xenopus optic tract, near the chiasma. J Embryol Exp Morphol 83: 1–14
Figdor MC, Stern CD (1993) Segmental organization of embryonic diencephalon. Nature 363:630–634
Fitzgibbon T, Reese BE (1992) Position of growth cones within the retinal nerve fibre layer of fetal ferrets. J Comp Neurol 323: 153–166
Fitzgibbon T, Reese BE (1996) Organization of retinal ganglion cell axons in the optic fiber layer and nerve of fetal ferrets. Vis Neurosci 13: 847–861
Frisen J, Yates PA, McLaughlin T, Friedman GC, O’Leary DD, 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: 235–243
Godement P, Salaun J, Mason CA (1990) Retinal axon pathfinding in the optic chiasm: divergence of crossed and uncrossed fibers. Neuron 5: 173–186
Godement P, Wang LC, Mason CA (1994) Retinal axon divergence in the optic chiasm: dynamics of growth cone behavior at the midline [published erratum appears in J Neurosci 1995 Mar; 15(3 Pt 1): following table of contents]. J Neurosci 14: 7024–7039
Guillery RW (1971) An abnormal retinogeniculate projection in the albino ferret (Mustela furo). Brain Res 33: 482–485
Guillery RW, Hickey TL, Kaas JH, Felleman DJ, Debruyn EJ, Sparks DL (1984) Abnormal central visual pathways in the brain of an albino green monkey (Cercopithecus aethiops). J Comp Neurol 226: 165–183
Guillery RW, Jeffery G, Cattanach BM (1987) Abnormally high variability in the uncrossed retinofugal pathway of mice with albino mosaicism. Development 101: 857–867
Guillery RW, Jeffery G, Saunders N (1999) Visual abnormalities in albino wallabies: a brief note. J Comp Neurol 403: 33–38
Guillery RW, Okoro AN, Witkop CJ, Jr (1975) Abnormal visual pathways in the brain of a human albino. Brain Res 96: 373–377
Guillery RW, Updyke BV (1976) Retinofugal pathways in normal and albino axolotls. Brain Res 109:235–244
Halfter W (1989) Antisera to basal lamina and glial endfeet disturb the normal extension of axons on retina and pigment epithelium basal laminae. Development 107:281–297
Halfter W (1996) Intraretinal grafting reveals growth requirements and guidance cues for optic axons in the developing avian retina. Dev Biol 177: 160–177
Halfter W, Deiss S (1986) Axonal pathfinding in organ-cultured embryonic avian retinae. Dev Biol 114: 296–310
Harris WA (1982) The transplantation of eyes to genetically eyeless salamanders: visual projections and somatosensory interactions. J Neurosci 2: 339–353
Harris WA (1989) Local positional cues in the neuroepithelium guide retinal axons in embryonic Xenopus brain. Nature 339: 218–221
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: 123–133
Herrick CJ (1941) Development of the optic nerves of Amblystoma. J Comp Neurol 74: 473–534
Holt CE (1989) A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. J Neurosci 9: 3123–3145
Holt CE, Harris WA (1993) Position, guidance, and mapping in the developing visual system. J Neurobiol 24: 1400–1422
Hopker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C (1999) Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401: 69–73
Hornberger MR, Dutting D, Ciossek T, Yamada T, Handwerker C, Lang S, Weth F, Huf J, Wessel R, Logan C, Tanaka H, Drescher U (1999) Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons. Neuron 22: 731–742
Hoskins SG (1986) Control of the development of the ipsilateral retinothalamic projection in Xenopus laevis by thyroxine: results and speculation. J Neurobiol 17: 203–229
Hoskins SG, Grobstein P (1984) Induction of the ipsilateral retinothalamic projection in Xenopus laevis by thyroxine. Nature 307: 730–733
Inoue A, Sanes JR (1997) Lamina-specific connectivity in the brain: regulation by N-cadherin, neurotrophins, and glycoconjugates. Science 276: 1428–1431
Jacobson M (1991) Developmental Neurobiology, pp. 776. New York: Plenum
Jeffery G, Kinsella B (1992) Translaminar deficits in the retinae of albinos. J Comp Neurol 326:637–644
Karlstrom RO, Trowe T, Klostermann S, Baier H, Brand M, Crawford AD, Grunewald B, Haffter P, Hoffmann H, Meyer SU, Muller BK, Richter S, van Eeden FJ, Nusslein-Volhard C, Bonhoeffer F (1996) Zebrafish mutations affecting retinotectal axon pathfinding. Development 123:427–438
Leppert CA, Diekmann H, Paul C, Laessing U, Marx M, Bastmeyer M, Stuermer CA (1999) Neurolin Ig domain 2 participates in retinal axon guidance and Ig domains 1 and 3 in fasciculation. J Cell Biol 144: 339–349
Lilienbaum A, Reszka AA, Horwitz AF, Holt CE (1995) Chimeric integrins expressed in retinal ganglion cells impair process outgrowth in vivo. Mol Cell Neurosci 6: 139–152
Lohof AM, Quillan M, Dan Y, Poo MM (1992) Asymmetric modulation of cytosolic cAMP activity induces growth cone turning. J Neurosci 12: 1253–1261
Maggs A, Scholes J (1986) Glial domains and nerve fiber patterns in the fish retinotectal pathway. J Neurosci 6: 424–438
Marcus RC, Blazeski R, Godement P, Mason CA (1995) Retinal axon divergence in the optic chiasm: uncrossed axons diverge from crossed axons within a midline glial specialization. J Neurosci 15: 3716–3729
Mason CA, Marcus RC, Wang LC (1996) Retinal axon divergence in the optic chiasm: growth cone behaviors and signalling cells. Prog Brain Res 108: 95–107
Mason CA, Sretavan DW (1997) Glia, neurons, and axon pathfinding during optic chiasm development. Curr Opin Neurobiol 7: 647–653
Mason CA, Wang LC (1997) Growth cone form is behavior-specific and, consequently, positionspecific along the retinal axon pathway. J Neurosci 17: 1086–1100
Mastick GS, Davis NM, Andrew GL, Easter SS, Jr. (1997) Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain. Development 124: 1985–1997
McFarlane S, Cornel E, Amaya E, Holt CE (1996) Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition. Neuron 17: 245–254
McFarlane S, McNeill L, Holt CE (1995) FGF signaling and target recognition in the developing Xenopus visual system. Neuron 15: 1017–1028
Miskevich F, Zhu Y, Ranscht B, Sanes JR (1998) Expression of multiple cadherins and catenins in the chick optic tectum. Mol Cell Neurosci 12: 240–255
Monschau B, Kremoser C, Ohta K, Tanaka H, Kaneko T, Yamada T, Handwerker C, Hornberger MR, Loschinger J, Pasquale EB, Siever DA, Verderame MF, Muller BK, Bonhoeffer F, Drescher U (1997) Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. Embo J 16: 1258–1267
Ohta K, Tannahill D, Yoshida K, Johnson AR, Cook GM, Keynes RJ (1999) Embryonic lens repels retinal ganglion cell axons. Dev Biol 211: 124–132
Ott H, Bastmeyer M, Stuermer CA (1998) Neurolin, the goldfish homolog of DM-GRASP, is involved in retinal axon pathfinding to the optic disk. J Neurosci 18: 3363–3372
Picker A, Brennan C, Reifers F, Clarke JD, Holder N, Brand M (1999) Requirement for the zebrafish mid-hindbrain boundary in midbrain polarisation, mapping and confinement of the retinotectal projection. Development 126: 2967–2978
Raper JA, Grunewald EB (1990) Temporal retinal growth cones collapse on contact with nasal retinal axons. Exp Neurol 109: 70–74
Reese BE, Baker GE (1993) The re-establishment of the representation of the dorso-ventral retinal axis in the chiasmatic region of the ferret. Vis Neurosci 10: 957–968
Reifers F, Bohli H, Walsh EC, Crossley PH, Stainier DY, Brand M (1998) Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125: 2381–2395
Retaux S, Harris WA (1996) Engrailed and retinotectal topography. Trends Neurosci 19: 542–546
Riehl R, Johnson K, Bradley R, Grunwald GB, Cornel E, Lilienbaum A, Holt CE (1996) Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17: 837–848
Roskies A, Friedman GC, O’Leary DD (1995) Mechanisms and molecules controlling the development of retinal maps. Perspect Dev Neurobiol 3: 63–75
Scholes JH (1979) Nerve fibre topography in the retinal projection to the tectum. Nature 278: 620–624
Shamim H, Mahmood R, Logan C, Doherty P, Lumsden A, Mason I (1999) Sequential roles for Fgf4, En 1 and Fgf8 in specification and regionalisation of the midbrain. Development 126: 945–959
Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Nat Acad Sci 50: 703–710
Sretavan DW, Kruger K (1998) Randomized retinal ganglion cell axon routing at the optic chiasm of GAP-43-deficient mice: association with midline recrossing and lack of normal ipsilateral axon turning. J Neurosci 18: 10502–10513
Sretavan DW, Pure E, Siegel MW, Reichardt LF (1995) Disruption of retinal axon ingrowth by ablation of embryonic mouse optic chiasm neurons. Science 269: 98–101
Stone KE, Sakaguchi DS (1996) Perturbation of the developing Xenopus retinotectal projection following injections of antibodies against betal integrin receptors and N-cadherin. Dev Biol 180: 297–310
Taylor JS (1987) Fibre organization and reorganization in the retinotectal projection of Xenopus. Development 99: 393–410
Taylor JS (1991) The early development of the frog retinotectal projection. Development Suppl 95–104
Thanos S, Bonhoeffer F, Rutishauser U (1984) Fiber-fiber interaction and tectal cues influence the development of the chicken retinotectal projection. Proc Natl Acad Sci USA 81: 1906–1910
Trowe T, Klostermann S, Baier H, Granato M, Crawford AD, Grunewald B, Hoffmann H, Karlstrom RO, Meyer SU, Muller B, Richter S, Nusslein-Volhard C, Bonhoeffer F (1996) Mutations disrupting the ordering and topographic mapping of axons in the retinotectal projection of the zebrafish, Danio rerio. Development 123: 439–450
Tuttle R, Braisted JE, Richards LJ, O’Leary DD (1998) Retinal axon guidance by region-specific cues in diencephalon. Development 125: 791–801
Walz A, McFarlane S, Brickman YG, Nurcombe V, Bartlett PF, Holt CE (1997) Essential role of heparan sulfates in axon navigation and targeting in the developing visual system. Development 124: 2421–2430
Wang LC, Dani J, Godement P, Marcus RC, Mason CA (1995) Crossed and uncrossed retinal axons respond differently to cells of the optic chiasm midline in vitro. Neuron 15: 1349–1364
Webster MJ, Rowe MH (1991) Disruption of developmental timing in the albino rat retina. J Comp Neurol 307: 460–474
Wilson SW, Placzek M, Furley AJ (1993) Border disputes: do boundaries play a role in growthcone guidance? Trends Neurosci 16: 316–323
Yamagata M, Herman JP, Sanes JR (1995) Lamina-specific expression of adhesion molecules in developing chick optic tectum. J Neurosci 15: 4556–4571
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2000 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Johnson, K.G., Harris, W.A. (2000). Connecting the Eye with the Brain: The Formation of the Retinotectal Pathway. In: Fini, M.E. (eds) Vertebrate Eye Development. Results and Problems in Cell Differentiation, vol 31. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-46826-4_9
Download citation
DOI: https://doi.org/10.1007/978-3-540-46826-4_9
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-53678-6
Online ISBN: 978-3-540-46826-4
eBook Packages: Springer Book Archive