Skip to main content
SpringerLink
Log in

Transformations of the retinal topography along the visual pathway of the chicken

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

It is still unclear how the retinotectal map of the chick is formed during development. In particular, it is not yet known whether or not the organization of fibres plays a role in the formation of this map. In order to contribute to the solution of this problem, we analysed the representation of the retinal topography at closely spaced intervals along the fibre pathway. We injected HRP into various sites of the tectal surface and traced the labelled fibre bundles back to the retina. The retinal topography was reconstructed at ten different levels, i.e. in the retina, the optic nerve head, the middle of the optic nerve, the chiasm (three levels), the optic tract (three levels), and the optic tectum. We obtained the following results: (1) The labelled fibre bundles as well as the fields of labelled retinal ganglion cells were always well delimited and coherent. (2) The reconstructions show that transformations of the retinal topography occur in the fibre pathway. The first and most important transformation is found in the optic nerve head where the retinal image is mirrored across an axis extending from dorsotemporal to ventronasal retina. In addition, the retinal representation is split in its temporal periphery. Thus, central and centrotemporal fibres are no longer in the centre of the image but close to the dorsal border of the nerve. Peripheral fibres are found along the medial, ventral and lateral circumference of the nerve. In the optic tract a second transformation occurs. The retinal topography is rotated clockwise by about 90 degrees and flattened to a band. The flattening is accompanied by a segregation of fibre bundles so that eventually central and centrotemporal retinal fibres are located centrally, ventral fibres dorsally and dorsal retinal fibres ventrally in the tract. By these two transformations an organization of fibres is produced in the optic tract which can be projected onto the tectal surface without major changes given that dorsal and ventral fibres remain in their relative positions, and that deep lying fibres project to the rostral and central tectum, superficial fibres to the caudal tectum.

The transformations which we have observed follow specific rules and thus maintain order in the pathway although retinotopy is lost. In conjunction with our earlier studies on the development of the retinotectal system we conclude that fibres are laid down in a chronotopic order. The transformations take place under particular structural constraints. Thus, an organization of fibres is provided in the optic tract which results in a retinotopic map when projected onto the tectal surface. This is stated for the order of magnitude of fibre bundles as investigated in this study. At the level of individual fibres additional factors may play an important role.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aebersold H, Creutzfeldt OD, Kuhnt U, Sanides D (1981) Representation of the visual field in the optic tract and optic chiasma of the cat. Exp Brain Res 42: 127–145

    Google Scholar 

  • Bernhardt R, Easter SS (1986) Map of retinal position onto the cross section of the optic pathway of goldfish. J Comp Neurol 254: 493–510

    Google Scholar 

  • Bunt SM (1982) Retinotopic and temporal organization of the optic nerve and tract in the adult goldfish. J Comp Neurol 206: 209–226

    Google Scholar 

  • Bunt SM, Horder TJ (1983) Evidence for an orderly arrangement of optic axons within the optic nerves of the major nonmammalian vertebrate classes. J Comp Neurol 213: 94–114

    Google Scholar 

  • Catsicas S, Thanos S, Clarke PGH (1987) Major role for neuronal death during brain development. Refinement of topographical connections. Proc Natl Acad Sci USA 84: 8165–8168

    Google Scholar 

  • Clarke PGH, Whitteridge D (1976) The projection of the retina, including the “red area’, on the optic tectum of the pigeon. Q J Exp Physiol 61: 351–358

    Google Scholar 

  • Cook JE, Horder TJ (1977) The multiple factors determining retinotopic order in the growth of optic fibres into the optic tectum. Phil Trans R Soc Lond B 278: 261–276

    Google Scholar 

  • Crossland WJ, Uchwat CJ (1979) Topographic projections of the retina and optic tectum upon the ventral lateral geniculate nucleus in the chick. J Comp Neurol 185: 87–106

    Google Scholar 

  • Crossland WJ, Cowan WM, Rogers LA, Kelly JP (1974) The specification of the retino-tectal projection in the chick. J Comp Neurol 155: 127–164

    Google Scholar 

  • Dawnay NAH (1979) ‘Chronotopic’ organization of goldfish optic pathway. J Physiol 296: 13–14P

    Google Scholar 

  • Ehrlich D, Mark R (1984) The course of axons of retinal ganglion cells within the optic nerve and tract of the chick (Gallus gallus). J Comp Neurol 223: 583–591

    Google Scholar 

  • Fawcett JW (1981) How axons grow down the Xenopus optic nerve. J Embryol Exp Morphol 65: 219–233

    Google Scholar 

  • Goldberg S (1974) Studies on the mechanics of development of the visual pathways in the chick embryo. Dev Biol 36: 24–43

    Google Scholar 

  • Graham RC, Karnovsky MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: Ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14: 291–302

    Google Scholar 

  • Halfter W, Deiss S, Schwarz U (1985) The formation of the axonal pattern in the embryonic avian retina. J Comp Neurol 232: 466–480

    Google Scholar 

  • Horder TJ, Mashkas A, Webb JN (1979a) Morphogenetic forces in the development of the avian retina of possible significance for the polarity of central visual projections. J Physiol (Lond) 291: 12–13P

    Google Scholar 

  • Horder TJ, Mashkas A, Pilgrim AJ (1979b) A method for the determination of fibre organization within the visual pathways of higher vertebrates. J Physiol 296: 8–9

    Google Scholar 

  • Horsburgh GM, Sefton AJ (1986) The early development of the optic nerve and chiasm in embryonic rat. J Comp Neurol 243: 547–560

    Google Scholar 

  • Horton JC, Greenwood MM, Hubel DH (1979) Non-retinotopic arrangement of fibres in cat optic nerve. Nature 282: 720–722

    Google Scholar 

  • LaVail JH, Cowan WM (1971a) The development of the chick optic tectum. I. Normal morphology and cytoarchitectonic development. Brain Res 28: 391–419

    Google Scholar 

  • LaVail JH, Cowan WM (1971b) The development of the chick optic tectum. II. Autoradiographic studies. Brain Res 28: 421–441

    Google Scholar 

  • Malsburg C von der, Willshaw DJ (1977) How to label nerve cells so that they can interconnect in an ordered fashion. Proc Natl Acad Sci USA 74: 5176–5178

    Google Scholar 

  • McGill JI, Powell TPS, Cowan WM (1966) The retinal representation upon the optic tectum and isthmo-optic nucleus in the pigeon. J Anat 100: 5–33

    Google Scholar 

  • McGraw CF, McLaughlin BJ (1980) Fine structural studies of synaptogenesis in the superficial layers of the chick optic tectum. J Neurocytol 9: 79–93

    Google Scholar 

  • McLoon SC (1985) Evidence for shifting connections during development of the chick retinotectal projection. J Neurosci 5: 2570–2580

    Google Scholar 

  • Mesulam M-M (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26: 106–117

    Google Scholar 

  • Meyer RL, Sperry RW (1976) Retino-tectal specificity: Chemoaffinity theory. In: Gottlieb G (ed) Neural and behavioral specificity. Studies on development of behavior and the nervous system, vol 3. Academic Press, New York, pp 111–149

    Google Scholar 

  • Polyak S (1957) The vertebrate visual system. University of Chicago Press, Chicago

    Google Scholar 

  • Rager G (1976a) Morphogenesis and physiogenesis of the retinotectal connection in the chicken. I. The retinal ganglion cells and their axons. Proc R Soc Lond B 192: 331–352

    Google Scholar 

  • Rager G (1976b) Morphogenesis and physiogenesis of the retino-tectal connection in the chicken. II. The retino-tectal synapses. Proc R Soc Lond B 192: 353–370

    Google Scholar 

  • Rager G (1978) Systems matching by degeneration. II. Interpretation of the generation and degeneration of retinal ganglion cells by a mathematical model. Exp Brain Res 33: 79–90

    Google Scholar 

  • Rager G (1980a) The development of the retinotectal projection in the chicken. Adv Anat Embryol Cell Biol, vol 63. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Rager G (1980b) Die Ontogenese der retinotopen Projektion. Beobachtung und Reflexion. Naturwissenschaften 67: 280–287

    Google Scholar 

  • Rager G (1983) Structural analysis of fibre organization during development. In: Changeux JP, Glowinski J, Imbert M, Bloom FE (eds) Molecular and cellular interactions underlying higher brain functions. Progress in Brain Res, vol 58. Elsevier, Amsterdam, pp 313–319

    Google Scholar 

  • Rager G, von Oeynhausen B (1979) Ingrowth and ramification of retinal fibres in the developing optic tectum of the chick embryo. Exp Brain Res 35: 213–227

    Google Scholar 

  • Rager G, Rager U (1978) Systems-matching by degeneration. I. A quantitative electronmicroscopic study of the generation and degeneration of retinal ganglion cells in the chicken. Exp Brain Res 33: 65–78

    Google Scholar 

  • Rager G, Rager U, Kabiersch A (1986) Organization of fibres in the retino-tectal pathway of the chick. Soc Neurosci (Abstr) 12(1): 436

    Google Scholar 

  • Rager G, Zimmermann C, Teckhaus L (1984) Zur Entwicklung des Gehirns. Dreidimensionale Rekonstruktionen mit dem Leitz T.A.S. Leitz Mitt. Wiss Tech VIII.7: 202–207

    Google Scholar 

  • Reh TA, Pitts E, Constantine-Paton M (1983). The organization of the fibers in the optic nerve of normal and tectum-less Rana pipiens. J Comp Neurol 218: 282–296

    Google Scholar 

  • Rusoff AC, Easter SS (1980) Order in the optic nerve of gold-fish. Science 208: 311–312

    Google Scholar 

  • Sanderson KJ (1971) Visual field projection columns and magnification factors in the lateral geniculate nucleus of the cat. Exp Brain Res 13: 280–287

    Google Scholar 

  • Scalia F, Arango V (1982) The anti-retinotopic organization of the frog's optic nerve. Brain Res 266: 121–126

    Google Scholar 

  • Scholes JH (1979) Nerve fibre topography in the retinal projection to the tectum. Nature 278: 620–624

    Google Scholar 

  • Sperry RW (1943) Visuomotor coordination in the newt (Triturus viridescens) after regeneration of the optic nerve. J Comp Neurol 79: 33–55

    Google Scholar 

  • Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 50: 703–710

    Google Scholar 

  • Springer AD, Mednick AS (1985) Topography of the goldfish optic tracts: Implications for the chronological clustering model. J Comp Neurol 239: 108–116

    Google Scholar 

  • Springer AD, Mednick AS (1986) Simple and complex retinal ganglion cell axonal rearrangement of the optic chiasm. J Comp Neurol 247: 233–245

    Google Scholar 

  • Taylor JSH (1987) Fibre organization and reorganization in the retinotectal projection of Xenopus. Development 99: 393–410

    Google Scholar 

  • Teckhaus L, Lübbers DW, Rager G (1979) A new method of three-dimensional reconstruction of complicated structures by combining an automatic and interactive computer technique. Microscopica Acta (Suppl) 3: 235–240

    Google Scholar 

  • Thanos S, Bonhoeffer F (1983) Investigations on the development and topographic order of retinotectal axons: Anterograde staining of axons and perikarya with rhodamine in vivo. J Comp Neurol 219: 420–430

    Google Scholar 

  • Thanos S, Bonhoeffer F (1987) Axonal arborization in the developing chick retinotectal system. J Comp Neurol 261: 155–164

    Google Scholar 

  • 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 81: 1906–1910

    Google Scholar 

  • Torrealba F, Guillery RW, Eysel U, Polley EH, Mason CA (1982) Studies of retinal representations within the cat's optic tract. J Comp Neurol 211: 377–396

    Google Scholar 

  • Voigt T, Naito J, Wässle H (1983) Retinotopic scatter of optic tract fibres in the cat. Exp Brain Res 52: 25–33

    Google Scholar 

  • Walsh C, Guillery RW (1985) Age-related fiber order in the optic tract of the ferret. J Neurosci 5: 3061–3069

    Google Scholar 

  • Willshaw DJ, von der Malsburg C (1976) How patterned neural connections can be set up by self-organization. Proc R Soc Lond B 194: 431–445

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Anatomy, University of Fribourg, Rue Gockel 1, CH-1700, Fribourg, Switzerland

    Ute Rager, Günter Rager & Alexa Kabiersch

Authors
  1. Ute Rager
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Günter Rager
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexa Kabiersch
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rager, U., Rager, G. & Kabiersch, A. Transformations of the retinal topography along the visual pathway of the chicken. Anat Embryol 179, 135–148 (1988). https://doi.org/10.1007/BF00304695

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00304695

Key words

Search

Navigation