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Development of geniculocortical axon arbors in a primate

Published online by Cambridge University Press:  02 June 2009

S. L. Florence  and
V. A. Casagrande
S. L. Florence
Affiliation:
Departments of Cell Biology and Psychology, Vanderbilt University, Nashville
V. A. Casagrande
Affiliation:
Departments of Cell Biology and Psychology, Vanderbilt University, Nashville
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Abstract

The main objective of the present study was to describe the postnatal development of magnocellular and parvocellular LGN axons within the primate striate cortex. For this purpose, we bulk labeled axons in neonatal prosimians (galagos) in vivo or in vitro at regular intervals from birth (PO) to 12 weeks after birth by injecting horseradish peroxidase (HRP) into white matter anterior to the striate cortex. Filled axons within layer IV were reconstructed, quantitatively analyzed, and compared to a population of adult axons described previously (Florence & Casagrande, 1987).

Our results show that although axons are morphologically immature at birth, they are restricted to the upper (IVα) and lower (IVβ) tiers of layer IV of the striate cortex as in adults. In adults, we referred to the presumed magnocellular LGN axons terminating in IVα as type I and the presumed parvocellular axons terminating in IVβ as type II. We used the same convention for developing axons.

From birth to 3 weeks postnatal, type I and II axon classes are more variable in appearance than adult counterparts, and are not morphologically class distinct. As axons mature, parent axon shafts increase in caliber, arbors become smaller and more radial, and other immature features (e.g. spikes, protrusions, growth cones) are less evident. Both arbor classes mature slowly and some still exhibit immature features (e.g. growth cones) as late as 12 weeks postnatally. Although arbors do not show class-distinctive features until late in development, each class does show some unique maturational trends. Type I arbors are only slightly larger than adult counterparts at birth, whereas type II arbors are dramatically larger. Type I arbors increase in branch complexity with age, whereas type II arbors simply show a shift in complexity toward the center of the arbor with decreasing size over time. These growth trends suggest that magnocellular and parvocellular pathways to cortex could be differentially vulnerable to the manipulation of postnatal visual experience.

Keywords

PrimateGeniculocortical axonsParallel pathwaysDevelopment
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 3 , September 1990 , pp. 291 - 309
Copyright
Copyright © Cambridge University Press 1990

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References

Anker, R.L. & Cragg, B.G. (1974). Development of the extrinsic connections of the visual cortex of the cat. Journal of Comparative Neurology 154, 29–42.Google Scholar
Blakemore, C. & Van Sluyters, R.C. (1974). Reversal of physiological effects of monocular deprivation in kittens: further evidence for a sensitive period. Journal of Physiology 237, 195–216.CrossRefGoogle ScholarPubMed
Blasdell, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389–1413.CrossRefGoogle Scholar
Carey, R.G., Fitzpatrick, D. & Diamond, I.T. (1979). Layer I of striate cortex of Tupaia gus and Galago senegalensis: projections from thalamus and claustrum revealed by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 186, 393–438.Google Scholar
Casagrande, V.A. & DeBruyn, E.J. (1982). The galago visual system: aspects of normal organization and developmental plasticity. In The Lesser Bushbaby as an Animal Model: Selected Topics, ed. Haines, D., pp. 107–135. Boca Raton, Florida: CRC Press, Incorporated.Google Scholar
Casagrande, V.A. & Joseph, R. (1980). Morphologic effects of monocular deprivation and recovery on the dorsal lateral geniculate nucleus in galago. Journal of Comparative Neurology 194, 413–426.CrossRefGoogle ScholarPubMed
Casagrande, V.A., Irvin, G.E., Norton, T.T., Sesma, M.A. & Petry, H.M. (1986). Difference of Gaussians model of CSF's from W-, X-, and Y-like cells in primate LGN. Investigative Ophthalmology and Visual Science (Suppl.) 27, 16.Google Scholar
Casagrande, V.A. & Skeen, L.C. (1980). Organization of ocular dominance columns in galago demonstrated by autoradiographic and deoxyglucose methods. Society for Neuroscience Abstracts 6, 315.Google Scholar
Conley, M., Birecree, E. & Casagrande, V.A. (1985). Neuronal classes and their relation to functional and laminar organization of the lateral geniculate nucleus: a Golgi study of the prosimian primate, Galago crassicaudatus. Journal of Comparative Neurology 242, 561–583.Google Scholar
Diamond, I.T., Conley, M., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584–610.Google Scholar
Florence, S.L. & Casagrande, V.A. (1984). Postnatal development of geniculostriate axons in galagos. Society for Neuroscience Abstract 10, 142.Google Scholar
Florence, S.L. & Casagrande, V.A. (1987). The organization of individual afferent axons in layer IV of striate cortex of a primate (Galago dsenegalensis). Journal of Neuroscience 7, 3850–3868.Google Scholar
Friedlander, M.J. & Martin, K.A.C. (1989). Development of Y-axon innervation of cortical area 18 in the cat. Journal of Physiology 416, 183–213.Google Scholar
Glendenning, K.K., Kofron, E.A. & Diamond, I.T. (1976). Laminar organization of projections of the lateral geniculate nucleus to the striate cortex in galago. Brain Research 105, 538–546.Google Scholar
Hässler, R. (1967). Comparative anatomy of central visual systems in day- and night-active primates. In Evolution of the Forebrain, ed. Hässler, R. & Stephen, H., pp. 419–434. New York: Plenum Press.Google Scholar
Hubel, D.H., Wiesel, T.N. & LeVay, S. (1977). Plasticity of oculardominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society (London) 278, 377–409.Google Scholar
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like receptive-field properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254–270.CrossRefGoogle ScholarPubMed
Joseph, R. & Casagrande, V.A. (1980). Visual deficits and recovery following monocular lid closure in a prosimian primate. Behavioral Brain Research 1, 165–186.Google Scholar
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus in primates. Journal of Comparative Neurology 182, 517–554.Google Scholar
Kato, N., Kawaguchi, S., Yamamoto, T., Samejima, A. & Miyata, H. (1983). Postnatal development of the geniculocortical projection in the cat: electrophysiological and morphological studies. Experimental Brain Research 51, 65–72.CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1988). Development of primate retinogeniculate axon arbors. Visual Neuroscience 1, 103–123.CrossRefGoogle ScholarPubMed
Lachica, E., Florence, S., Crooks, M. & Casagrande, V.A. (1989). The morphology of geniculocortical axon arbors in a monocularly deprived primate. Investigative Ophthalmology and Visual Science (Suppl.) 30, 30.Google Scholar
Lachica, E.A., Crooks, M.W. & Casagrande, V.A. (1990). The effects of monocular deprivation on the morphology of retinogeniculate axon arbors in a primate. Journal of Comparative Neurology 296, 303–323.CrossRefGoogle ScholarPubMed
Laemle, L., Benhamida, C. & Purpura, D.P. (1972). Laminar distribution of geniculocortical afferents in visual cortex of the postnatal kitten. Brain Research 41, 25–37.Google Scholar
LeVay, S. & Staryker, M.P. (1978). The development of ocular dominance columns in the cat. In Society of Neurosciences Symposium, 4: Aspects of Developmental Neurobiology, ed. Ferendelli, J., pp. 83–98. Bethesda, Maryland: Society of Neurosciences.Google Scholar
LeVay, S., Stryker, M.P. & Shatz, C.J. (1978). Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study. Journal of Comparative Neurology 179, 223–244.Google Scholar
LeVay, S., Wiesel, T.N. & Hubel, D.H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. Journal of Comparative Neurology 191, 1–51.CrossRefGoogle ScholarPubMed
Mason, C.A. & Gregory, E. (1984). Postnatal maturation of cerebellar mossy and climbing fibers: transient expression of dual features on single axons. Journal of Neuroscience 4, 1715–1735.CrossRefGoogle ScholarPubMed
Movshon, J.A. & Van Sluyters, R.C. (1981). Visual neural development. Annual Review of Psychology 32, 477–522.Google Scholar
Naegele, J.R., Jhaveri, S. & Schneider, G.E. (1988). Sharpening of topographical projections and maturation of geniculocortical axon arbors in the hamster. Journal of Comparative Neurology 277, 593–607.Google Scholar
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in the lateral geniculate nucleus of bush-baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715–741.Google Scholar
Norton, T.T., Casagrande, V.A., Irvin, G.E., Sesma, M.A. & Petry, H.M. (1988). Contrast sensitivity functions of W-, X-, and Y-like relay cells in the lateral geniculate nucleus of bushbaby (Galago crassicaudatus). Journal of Neurophysiology 59, 1639–1656.Google Scholar
O'Kusky, J. & Colonnier, M. (1982). Postnatal changes in the number of neurons and synapses in the visual cortex (area 17) of the macaque monkey: a stereologic analysis in normal and monocularly deprived animals. Journal of Comparative Neurology 210, 291–306.Google Scholar
Rakic, P. (1977). Prenatal development of the visual system in rhesus monkey. Philosophical Transactions of the Royal Society (London) 278, 245–260.Google ScholarPubMed
Scoll, D.A. (1955). The organization of visual cortex in the cat. Journal of Anatomy 89, 33–46.Google Scholar
Sesma, M.A., Irvin, G.E., Kuyk, T.K., Norton, T.T. & Casagrande, V.A. (1984). Effects of monocular deprivation on the lateral geniculate nucleus in a primate. Proceedings of the National Academy of Sciences of the U.S.A. 81, 2255–2259.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738–855.Google Scholar
Sretavan, D.W. & Shatz, C.J. (1986). Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus. Journal of Neuroscience 6, 234–251.Google Scholar
Weller, R.E. & Kaas, J.H. (1982). The organization of the visual system in galago. Comparisons with monkey. In The Lesser Bushbaby as an Animal Model, ed. Haines, D., pp. 107–135. Boca Raton, FL: CRC Press.Google Scholar