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Prenatal development of axon outgrowth and connectivity in the ferret visual system

Published online by Cambridge University Press:  02 June 2009

J. Kelly Johnson  and
V. A. Casagrande
J. Kelly Johnson
Affiliation:
Department of Cell Biology, Medical Center North C2310, Vanderbilt University, Nashville
V. A. Casagrande
Affiliation:
Department of Cell Biology, Medical Center North C2310, Vanderbilt University, Nashville Department of Psychology, Wilson Hall, Vanderbilt University, Nashville
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Abstract

The objective of this study was to determine when the retina, lateral geniculate nucleus (LGN), and striate cortex first send out axons, and first connect with each other, during embryonic development in the ferret. Specifically, we were interested in the timing relationship between axon outgrowth and known temporal patterns of neurogenesis in the LGN and striate cortex. Ferrets (Mustela putorius furo) were selected for study because of their immature developmental state in late gestation and relatively large litters.

We examined axon outgrowth from the retina, and anlagen of presumptive LGN and striate cortex between embryonic day 21–30 (E21–E30) using in situ inoculations of two fluorescent lipophilic dyes, Dil and DiA. Dil inoculations were made into the cortex and contralateral thalamus, and DiA inoculations were made into the contralateral eye. Retinal axon termination zones in the diencephalon following the DiA inoculations were used to validate the location of the LGN.

Visual cortex and LGN neurogenesis begins at E20 in ferrets. No axon outgrowth could be documented from retina or anlagen of striate cortex and LGN until E24. At E24 some retinal axons reach and cross the chiasm, cortical axons extend some distance within the cortical radiations, and thalamic axons are within the internal capsule. Retinogeniculate, geniculocortical, and corticogeniculate axons extend to their target structures by E27, as evidenced by retrograde labeling in cells of origin.

These data suggest that in the ferret retina, and developing LGN and striate cortex, (1) axon outgrowth from each visual area begins within 24-h of each other, after neurogenesis has begun at the source but before it is complete in the target; (2) axons may be generated before parent cell bodies have completed migration; and (3) arriving axons are in a position to influence target structures almost from their inception.

Keywords

NeurogenesisAxon outgrowthFetusMammalVisual system
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 1 , January 1993 , pp. 117 - 130
Copyright
Copyright © Cambridge University Press 1993

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References

Altman, J. & Bayer, S.A. (1979). Development of the diencephalon in the rat. VI. Re-evaluation of the embryonic development of the thalamus on the basis of thymidine-radiographic datings. Journal of Comparative Neurology 188, 501–524.CrossRefGoogle ScholarPubMed
Altman, J. & Bayer, S.A. (1989). Development of the rat thalamus: VI. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the lateral geniculate and lateral posterior nuclei. Journal of Comparative Neurology 284, 581–601.CrossRefGoogle ScholarPubMed
Bunt, S.M., Lund, R.D. & Land, P.W. (1983). Prenatal development of the optic projection in albino and hooded rats. Developmental Brain Research 6, 149–168.CrossRefGoogle Scholar
Casagrande, V.A. & Brunso-Bechtold, J.K. (1985). Critical events in lateral geniculate nucleus development. In Advances in Neurological and Behavioral Development, ed. Aslin, R.N., pp. 33–69. Norwood, New Jersey: Ablex.Google Scholar
Catalano, S.M., Robertson, R.T. & Killackey, H.P. (1991). Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2999–3003.CrossRefGoogle Scholar
Claps, A. & Casagrande, V.A. (1990). The distribution and morphology of corticogeniculate axons in ferrets. Brain Research 530, 126–129.CrossRefGoogle ScholarPubMed
Cohen, P.J. (1975). Signs and stages of anesthesia. In The Pharmacological Basis of Therapeutics, 5th ed., ed. Goodman, L.S. & GilMan, A., pp. 60–65, New York: Macmillan.Google Scholar
Cucchiaro, J. & Guillery, R.W. (1984). The prenatal development of the retinogeniculate pathways in normal and albino ferrets. Proceedings of the Royal Society B (London) 223, 141–164.Google Scholar
Ghosh, A. & Shatz, C.J. (1992). Pathfinding and target selection by developing geniculocortical axons. Journal of Neuroscience 12, 39–55.CrossRefGoogle ScholarPubMed
Godement, P., Vanselow, J., Thanos, S. & Bonhoeffer, F. (1987). A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101, 697–713.CrossRefGoogle ScholarPubMed
Greiner, J.V. & Weidman, T.A. (1981). Histogenesis of the ferret retina. Experimental Eye Research 33, 315–332.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Walsh, C. (1987). Changing glial organization relates to changing fiber order in the developing optic nerve of ferrets. Journal of Comparative Neurology 265, 203–217.CrossRefGoogle ScholarPubMed
Hickey, T.L. & Hitchcock, P.F. (1984). Genesis of neurons in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 228, 186–199.CrossRefGoogle ScholarPubMed
Honig, M. & Hume, R.I. (1989). Dil and DiO: Versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends in Neurosciences 12, 333–341.CrossRefGoogle ScholarPubMed
Hutchins, J.B. & Casagrande, V.A. (1990). Development of the lateral geniculate nucleus: Interactions between retinal afferent, cyto-architectonic, and glial cell process lamination in ferrets and tree shrews. Journal of Comparative Neurology 298, 113–128.CrossRefGoogle Scholar
Jackson, C.A., Peduzzi, J.D. & Hickey, T.L. (1989). Visual cortex development in the ferret. I. Genesis and migration of visual cortex neurons. Journal of Neuroscience 9, 1242–1253.CrossRefGoogle Scholar
Johnson, J.K. & Casagrande, V.A. (1992). Behavior of lipophilic dyes in the embryonic mammalian visual system. Society for Neuroscience Abstracts 18, 1126.Google Scholar
Johnson, J.K. & Casagrande, V.A. (1991). Transcellular diffusion events of the carbocyanine dye, DiA, in the embryonic ferret visual system. Society for Neuroscience Abstracts 17, 1133.Google Scholar
Johnson, J.K. & Chamberlain, S.C. Transneuronal diffusion of lipophilic dyes in the horseshoe crab visual system. Journal of Histochemistry and Cytochemistry (in press).Google Scholar
Law, M.I., Zahs, K.R. & Stryker, M.P. (1988). Organization of primary visual cortex (area 17) in the ferret. Journal of Comparative Neurology 278, 157–180.CrossRefGoogle ScholarPubMed
Linden, D.C., Guillery, R.W. & Cucchiaro, J. (1981). The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. Journal of Comparative Neurology 203, 189–211.CrossRefGoogle ScholarPubMed
Lund, R.D. & Mustari, M.J. (1977). Development of the geniculocortical pathway in rats. Journal of Comparative Neurology 173, 289–306.CrossRefGoogle ScholarPubMed
Luskin, M.B. & Shatz, C.J. (1985). Neurogenesis of the cat’s primary visual cortex. Journal of Comparative Neurology 242, 611–631.CrossRefGoogle ScholarPubMed
McConnell, S.K. & Levay, S. (1986). Anatomical organization of the visual system of the mink, Mustela vision. Journal of Comparative Neurology 250, 109–132.CrossRefGoogle Scholar
McConnell, S.K. & Shatz, C.J. (1988). Prenatal development of axonal projections from the cat’s visual cortex. Society for Neuroscience Abstracts 14, 743.Google Scholar
McConnell, S.K., Ghosh, A. & Shatz, C.J. (1989). Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245, 978–982.CrossRefGoogle ScholarPubMed
Meister, M., Wong, R.O.L., Baylor, D.A. & Shatz, C.J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943.CrossRefGoogle ScholarPubMed
Payne, B.R., Pearson, H.E. & Cornwell, P. (1988). Neocortical connections in fetal cats. Neuroscience Research 5, 513–543.CrossRefGoogle ScholarPubMed
Peduzzi, J.D. (1989). Neurogenesis of the geniculate nucleus in the ferret. Society for Neuroscience Abstracts 15, 1210.Google Scholar
Rakic, P. (1977). Prenatal development of the visual system in the rhesus monkey. Philosophical Transactions of the Royal Society B (London) 278, 245–260.Google ScholarPubMed
Rakic, P. (1979). Genesis of visual connections in the rhesus monkey. In Developmental Neurobiology of Vision, ed. Freeman, R.D., pp. 249–260. New York: Plenum.CrossRefGoogle Scholar
Robinson, S.R. & Dreher, B. (1990). The visual pathways of eutherian mammals and marsupials develop according to a common timetable. Brain, Behavior, and Evolution 36, 177–195.CrossRefGoogle ScholarPubMed
Rockland, K.S. (1985). Anatomical organization of primary visual cortex (area 17) in the ferret. Journal of Comparative Neurology 241, 225–236.CrossRefGoogle ScholarPubMed
Shatz, C.J. (1983). The prenatal development of the cat’s retinogeniculate pathway. Journal of Neuroscience 3, 482–499.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Kirkwood, P.A. (1984). Prenatal development of functional connections in the cat’s retinogeniculate pathway. Journal of Neuroscience 4, 1378–1397.CrossRefGoogle Scholar
Shatz, C.J. & Luskin, M.B. (1986). The relationship between the geniculocortical afferents and their cortical target cells during development of the cat’s primary visual cortex. Journal of Neuroscience 6, 3655–3668.CrossRefGoogle ScholarPubMed
Shatz, C.J., McConnell, S.K., Allendoerfer, K.L., Friauf, E. & Antonini, A. (1990). Pioneer neurons and target selection in cerebral cortical development. Cold Spring Harbor Symposia on Quantitative Biology 55, 469–480.CrossRefGoogle ScholarPubMed
Shatz, C.J. & Rakic, P. (1981). The genesis of efferent connections from the visual cortex of the fetal Rhesus monkey. Journal of Comparative Neurology 196, 287–307.CrossRefGoogle ScholarPubMed
Sheng, X.-M., Marotte, L.R. & Mark, R.F. (1990). Development of connections to and from the visual cortex in the wallaby (Macropus eugenii). Journal of Comparative Neurology 300, 196–200.CrossRefGoogle ScholarPubMed
So, K.-F., Schneider, G.E. & Frost, D.O. (1978). Postnatal development of retinal projections to the lateral geniculate body in Syrian hamsters. Brain Research 142, 343–352.CrossRefGoogle Scholar
Sutton, J.K. & Brunso-Bechtold, J.K. (1991). A Golgi study of dendritic development in the dorsal lateral geniculate nucleus of normal ferrets. Journal of Comparative Neurology 309, 71–85.CrossRefGoogle ScholarPubMed
Wye-Dvorak, J. (1984). Postnatal development of primary visual projections in the tammar wallaby (Macropus eugenii). Journal of Comparative Neurology 228, 491–508.CrossRefGoogle Scholar