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Development of primate retinogeniculate axon arbors

Published online by Cambridge University Press:  02 June 2009

Edward A. Lachica  and
Vivien A. Casagrande
Edward A. Lachica
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Vivien A. Casagrande
Affiliation:
Department of Psychology, Vanderbilt University, Nashville Department of Cell Biology, Vanderbilt University, School of Medicine, Nashville
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Abstract

In this study we examine the postnatal development of retinogeniculate axons projecting to the magnocellular (M axons), parvocellular (P axons), and koniocellular (K axons) layers of the lateral geniculate nucleus (LGN) in the prosimian primate, Galago crassicaudatus, in order to: (1) understand how individual retinogeniculate axons in primates mature postnatally, and (2) determine whether differences exist in the development of separate classes of axons that are known to be presynaptic to physiologically distinct cells in adults. In galagos, magnocellular, parvocellular, and koniocellular LGN layers contain Y-, X-, and W-like physiological cell classes, respectively (Norton & Casagrande, 1982).

In vitro and in vivo optic tract bulk injections of horseradish peroxidase (HRP) were made in animals ranging in age from the day of birth (P0) to adulthood. Two hundred and fifty axonal arbors were completely reconstructed from serial sections and examined qualitatively for general features of maturity and compared quantitatively for changes in shape, arbor width, area, volume, bouton number, and bouton density.

Our results confirm that in adult galagos M arbors are large and radially symmetric; P arbors are medium sized and elongated perpendicular to layer borders; K arbors are small and generally oriented parallel to layer borders. At birth, M, P, and K arbors, although still distinct and confined to layers, are qualitatively and quantitatively immature. Both the pattern and pace of maturation differ between classes. Overall, M arbors mature before P arbors which in turn mature before K arbors. Within classes, arbors representing central vision appear to develop about a week ahead of those representing peripheral vision; no differences are evident between the development of crossed and uncrossed arbors. In no case do arbors exhibit a period of postnatal exuberance, wherein arbors are larger than those of the adult as reported for cat X retinal axons. However, in width and bouton density P arbors are mature at P0 and thus occupy relatively more space in the nucleus compared to adult. All arbors mature rapidly and appear adult-like by the 4th or 5th postnatal week.

Keywords

DevelopmentRetinaLateral geniculate nucleusAxonPrimate
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 1 , January 1988 , pp. 103 - 123
Copyright
Copyright © Cambridge University Press 1988

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References

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 6, 775.CrossRefGoogle Scholar
Blasdel, G.G. & Fitzpatrick, D. (1984). Physiological organization of layer IV in macaque striate cortex. Journal of Neuroscience 4, 880–895.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Lund, J.S. (1983). Terminations of afferent axons in macque striate cortex. Journal of Neuroscience 3, 1389–1413.CrossRefGoogle Scholar
Bowling, D.B. & Michael, C.R. (1984). Terminal patterns of single, physiologically characterized optic tract fibers in the cat's lateral geniculate nucleus. Journal of Neuroscience 4, 198–216.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Joseph, R. (1980). Morphological effects of monocular deprivation and recovery on the dorsal lateral geniculate nucleus in galago. Journal of Comparative Neurology 194, 413–416.CrossRefGoogle ScholarPubMed
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.E., Boca Raton, Florida: CRC Press, Inc. pp. 137–168.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, 561–584.CrossRefGoogle ScholarPubMed
Conley, M., Penny, G.R. & Diamond, I.T. (1987). Terminations of individual optic tract fibers in the lateral geniculate nuclei of Galago crassicaudatus and Tupaia belangeri. Journal of Comparative Neurology 256, 71–87.CrossRefGoogle ScholarPubMed
Diamond, I.T., Conley, M.C., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584–610.CrossRefGoogle ScholarPubMed
Dreher, B., Fukuda, Y. & Rodieck, R.W. (1976). Identification, classification, and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old-world primates. Journal of Physiology (London) 258, 433–452.CrossRefGoogle ScholarPubMed
Florence, S.L., Sesma, M.A. & Casagrande, V.A. (1983). Morphology of geniculostriate afferents in a prosimian primate. Brain Research 270, 127–130.CrossRefGoogle Scholar
Florence, S.L. & Casagrande, V.A. (1984). Postnatal development of geniculostriate axons in galago. Society for Neuroscience Abstracts 10, 142.Google Scholar
Florence, S.L. & Casagrande, V.A. (1987). The organization of individual afferent axons in layer IV of striate cortex in a primate (Galago senegalensis). Journal of Neuroscience 7, 3850–3868.CrossRefGoogle Scholar
Friedlander, M.J., Stanford, L.R. & Sherman, S.M. (1982). Effects of monocular deprivation on the structure-function relationship of individual neurons in the cat's lateral geniculate nucleus. Journal of Neuroscience 2, 321–330.CrossRefGoogle ScholarPubMed
Garey, L.J. & Saini, K.D. (1981). Golgi studies of the normal development of neurons in the lateral geniculate nucleus of the monkey. Experimental Brain Research 44, 117–128.CrossRefGoogle ScholarPubMed
Garraghty, P.E., Sur, M., Weller, R.E. & Sherman, S.M. (1986 a). Morphology of retinogeniculate X and Y axon arbors in monocularly enucleated cats. Journal of Comparative Neurology 251, 198–215.CrossRefGoogle ScholarPubMed
Garraghty, P.E., Sur, M. & Sherman, S.M. (1986 b). Role of competitive interactions in the postnatal development of X and Y retinogeniculate axons. Journal of Comparative Neurology 251, 216–239.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1973). The effects of lid suture upon the growth of the cells in the dorsal lateral geniculate nucleus of kittens. Journal of Comparative Neurology 148, 417–422.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Weisel, T.N. (1972). Laminar and columnar distribution of geniculocortical fibers in macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like response 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. Behavioural Brain Research 1, 165–186.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R. (1982). X and Y cells in the lateral geniculate nucleus of the macaque monkey. Journal of Physiology 330, 125–143.CrossRefGoogle Scholar
Lachica, E.A., Condo, G.J., Conley, M. & Casagrande, V.A. (1986). Development of retinogeniculate axon arbors in a primate. Society for Neuroscience Abstracts 12, 589.Google Scholar
Lehmkuhle, S., Kratz, K.E., Mangel, S.C. & Sherman, S.M. (1980). Effects of early monocular lid suture on spatial and temporal sensitivity of neurons in dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 43, 542–556.CrossRefGoogle ScholarPubMed
Mason, C.A. (1982). Development of terminal arbors of retinogeniculate axons in the kitten. I. Light microscopical observations. Neuroscience 3, 541–559.CrossRefGoogle Scholar
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in lateral geniculate nucleus of bushbaby (Galago crassicaudatus). Journal of Neurophysiology 47, 715–741.CrossRefGoogle 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 bush baby (Galago crassicaudatus). Journal of Neurophysiology (in press).CrossRefGoogle Scholar
Rakic, P. (1977). Genesis of dorsal lateral geniculate nucleus in the monkey: site and time of origin, kinetics of proliferation, routes of migration, and pattern of distribution of neurons. Journal of Comparative Neurology 176, 23–52.CrossRefGoogle ScholarPubMed
Reese, B.E. & Guillery, R.W. (1987). Distribution of axons according to diameter in the moneky's optic tract. Journal of Comparative Neurology 260, 453–460.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–797.CrossRefGoogle ScholarPubMed
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, National Academy of Science 81, 2255–2259.CrossRefGoogle Scholar
Shatz, C.J. & Sretavan, D.W. (1986). Interactions between retinal ganglion cells during the development of the mammalian visual system. Annual Review of Neuroscience 9, 171–209.CrossRefGoogle ScholarPubMed
Sherman, S.M., Hoffman, K.P. & Stone, J. (1972). Loss of a specific cell type from the dorsal lateral geniculate nucleus in visually deprived cats. Journal of Neurophysiology 35, 532–541.CrossRefGoogle ScholarPubMed
Sherman, S.M., Wilson, J.R., Kaas, J.H. & Webb, S.V. (1976). X-and Y-cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). Science 192, 475–476.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Review 62, 738–855.CrossRefGoogle ScholarPubMed
Sherman, S.M. (1985). Development of retinal projections to the cat's lateral geniculate nucleus. Trends in NeuroScience 8, 350–355.CrossRefGoogle Scholar
Sretavan, D.W. & Shatz, C.J. (1984). Prenatal development of individual retinogeniculate axons during the period of segregation. Nature 308, 845–848.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Sur, M. & Sherman, S.M. (1982). Retinogeniculate terminations in the cat: morphological differences between X- and Y-cell axons. Science 218, 389–391.CrossRefGoogle Scholar
Sur, M., Humphrey, A.L. & Sherman, S.M. (1982). Monocular deprivation effects X- and Y-cell retinogeniculate terminations in cats. Nature 300, 183–185.CrossRefGoogle ScholarPubMed
Sur, M., Weller, R.E. & Sherman, S.M. (1984). Development of X-and Y-cell retinogeniculate terminations in kittens. Nature 310, 246–249.CrossRefGoogle ScholarPubMed
Sur, M., Garraghty, P.E. & Stryker, M.P. (1985). Morphology of physiologically identified retinogeniculate axons in cats following blockade of retinal impulse activity. Society for Neuroscience Abstracts 11, 805.Google Scholar
Sur, M. (1987). Development and plasticity of retinal X and Y axon terminations in the cat's lateral geniculate nucleus. Brain, Behavior, and Evolution (in press).Google Scholar
Sur, M., Esguerra, M., Garraghty, P.E., Knitzer, M.F. & Sherman, S.M. (1987). Morphology of physiologically identified retinogeniculate X- and Y-axons in the cat. Journal of Neurophysiology 58, 1–32.CrossRefGoogle ScholarPubMed
Vital-Durand, R., Garey, L.J. & Blakemore, C. (1978). Monocular and binocular deprivation in the monkey: morphological effects and reversibility. Brain Research 158, 45–64.CrossRefGoogle ScholarPubMed
Von Noorden, G.K. & Middleditch, P.R. (1975). Histology of monkey's lateral geniculate nucleus after unilateral lid closure and experimental strabismus: further observations. Investigative Ophthalmology and Visual Sciences 14, 674–683.Google ScholarPubMed
Walsh, C. & Polley, E.H. (1985). The topography of ganglion cell production in the cat's retina. Journal of Neuroscience 5, 741–750.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1982). The organization of the visual system in galago: comparisons with monkeys. In The Lesser Bush Baby as a Laboratory Animal, ed. Haines, D.E., Boca Raton, Florida: CRC Press, Inc. pp. 108–136.Google Scholar
Winer, B.J. (1971). Statistical Principles in Experimental Design, 2nd ed. New York: McGraw-Hill.Google Scholar