Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-19T10:55:00.070Z Has data issue: false hasContentIssue false
  • English
  • Français

The postnatal development of geniculocortical axon arbors in owl monkeys

Published online by Cambridge University Press:  02 June 2009

Marcie W. Pospichal ,
Sherre L. Florence  and
Jon H. Kaas
Marcie W. Pospichal
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Sherre L. Florence
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Jon H. Kaas
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Get access Rights & Permissions [Opens in a new window]

Abstract

To characterize the postnatal development of geniculocortical axon arbor morphology in owl monkeys at a series of ages from birth to adulthood, individual arbors were bulk-filled with HRP in brain slice preparations and were reconstructed from serial sections. At all ages, cortical layers and sublayers were obvious. Presumed M or magnocellular arbors were largely confined to layer IVα, but they also extended into layer IIIc (IVB of Brodmann, 1909); presumed P or parvocellular arbors were almost exclusively confined to layer IVβ. Other axons that may reflect feedback projections from MT terminated in layer IIIc. Overall, M axon arbors increased in size and complexity from birth to adulthood with mean surface-view arbor areas ranging from 0.08 ± 0.01 mm2 in newborns to 0.24 ± 0.02 mm2 in adults. The developing P arbor areas were, on average, as large or larger than adult (newborn = 0.07 ± 0.01 mm2, adult = 0.047 ± 0.01 mm2; n.s.) but the arbors were somewhat less complex. Since the brain and area 17 increase in size postnatally, the proportion of area 17 subserved by each P arbor would decrease in postnatal development. Terminal boutons with immature features were evident in both M and P populations at all developmental ages. The results indicate that, while both LGN axon types in monkeys undergo morphological changes postnatally, M arbors appear to mature by increasing arbor size and terminal branching complexity, whereas P arbors increase in complexity but not in size. These distinct programs of axon arbor development suggest that the periods of susceptibility of geniculocortical axon arbors to postnatal influences of the environment, and the types of plastic responses they potentially exhibit, are class-specific.

Keywords

PrimateGeniculocortical axon arborsStriate cortexDevelopment
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 71 - 90
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, J.C. (1977). Technical consideration in the use of horseradish peroxidase as a neuronal marker. Neuroscience 2, 141–145.CrossRefGoogle ScholarPubMed
Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction products. Journal of Histochemical Cytochemistry 29, 775.CrossRefGoogle Scholar
Allman, J.M. & Kaas, J.H. (1974). The organization of the second visual area (V II) in the owl monkey: A second-order transformation of the visual hemifield. Brain Research 76, 247–265.CrossRefGoogle Scholar
Anderson, J.C., DeHay, C., Friedlander, M.J., Martin, K.A.C. & Nelson, J.C. (1992). Synaptic connections of physiologically identified geniculocortical axons in kitten cortical area 17. Proceedings of the Royal Society (London) 250, 187–194.Google ScholarPubMed
Blakemore, C. & Vital-Durand, F. (1986). Organization and postnatal development of the monkey’s lateral geniculate nucleus. Journal of Physiology 380, 453–491.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Lund, J.S. (1983). Terminations of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389–1413.CrossRefGoogle ScholarPubMed
Boothe, R.G., Dobson, V. & Teller, D.Y. (1985). Postnatal development of vision in human and nonhuman primates. Annual Review in Neuroscience 8, 495–545.CrossRefGoogle ScholarPubMed
Brodmann, K. (1909). Vergleichends Lokalizationlehre der Grosshirnrinde. Barth: Leipzig.Google Scholar
Bullier, J. & Henry, G.H. (1979). Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. Journal of Comparative Neurophysiology 182, 1271–1281.CrossRefGoogle Scholar
Casagrande, V.A. & Norton, J.T. (1991 a). Lateral geniculate nucleus: A review of its physiology and function. In Electrophysiology of Vision, ed. Leventhal, A.G.Google Scholar
Casagrande, V.A. & Norton, J.T. (1991 b). Lateral geniculate nucleus: A review of its physiology and function. In The Neural Basis of Vision Function: Vision and Vision Dysfunction, ed. Leventhal, A.G., pp. 41–84. London: McMillan Press, Ltd.Google Scholar
Chino, Y.M., Kaas, J.H., Smith, E.L. III, Langston, A.L. & Cheng, H. (1992). Rapid reorganization of cortical maps in adult cats following restricted deafferentations in retina. Vision Research 32, 789–796.CrossRefGoogle ScholarPubMed
Connolly, M. & Van Essen, D.C. (1984). The representation of the visual field in parvicellular and magnocellular laminae of the lateral geniculate nucleus in the macaque monkey. Journal of Comparative Neurology 226, 544–564.CrossRefGoogle ScholarPubMed
Cusick, C.G., Gould, H.J. III & Kaas, J.H. (1984). Interhemispheric connections of visual cortex of owl monkeys (Aotus trivirgatus), marmosets (Callithrix jacchus), and galagos (Galago crassicaudalus). Journal of Comparative Neurology 230, 311–336.CrossRefGoogle ScholarPubMed
Dekaban, A.S. & Sadowsky, D. (1978). Changes in brain weights during the span of human life: Relation of brain weights to body heights and body weights. Annals of Neurology 4, 345.CrossRefGoogle ScholarPubMed
Diamond, I.T., Conley, M., Itoh, K. & Fitzgerald, D. (1985). Laminar organization of geniculocortical projections in Galago senegalensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584–610.CrossRefGoogle ScholarPubMed
Dixson, A.F. & Fleming, D. (1981). Parental behavior and infant development in owl monkeys (Aotus trivirgatus griseimembra). Journal of Zoology (London) 194, 25–99.CrossRefGoogle Scholar
Dreher, B., Fukada, 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 258, 433–452.CrossRefGoogle ScholarPubMed
Ferster, D. & LeVay, S. (1978). The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat. Journal of Comparative Neurology 182, 923–944.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neuroscience 3, 673–702.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S. & Blasdel, G.G. (1985). Intrinsic connections of macaque striate cortex: Afferent and efferent connections of lamina 4C. Journal of Neuroscience 5, 3329–3346.CrossRefGoogle ScholarPubMed
Fitzpatrick, D. & Raczkowski, D. (1990). Innervation patterns of single physiologically identified geniculocortical axons in the striate cortex of the tree shrew. Proceedings of the National Academy of Sciences of the U.S.A. 87, 449–453.CrossRefGoogle ScholarPubMed
Florence, S.L. & Casagrande, V.A. (1987). Organization of individual afferent axons in layer IV of striate cortex in a primate. Visual Neuroscience 5, 3850–3868.Google Scholar
Florence, S.L. & Casagrande, V.A. (1990). The development of geniculocortical axon arbors in a primate. Visual Neuroscience 7, 291–309.CrossRefGoogle Scholar
Florence, S.L. & Kaas, J.H. (1992). Ocular-dominance columns in area 17 of Old World macaque and talapoin monkeys: Complete reconstructions and quantitative analyses. Visual Neuroscience 8, 449–462.CrossRefGoogle ScholarPubMed
Freund, T.F., Martin, K.A.C., Soltesz, I., Somogyi, P. & Whitteridge, D. (1989). Arborization patterns and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey. Journal of Comparative Neurology 289, 315–336.CrossRefGoogle ScholarPubMed
Garraghty, P.E., Kaas, J.H. & Florence, S.L. (1993). Plasticity of sensory and motor maps in adult and developing mammals. In Advances in Neural and Behavioral Development, Vol. 4, ed. Casagrande, V.A. & Shinkman, P.S.Norwood, New Jersey: Ablex Publishing Corp. (in press).Google Scholar
Gilbert, C.D. (1992). Horizontal integration and cortical dynamics. Neuron 9, 1–13.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Weisel, T.N. (1992). Receptive-field dynamics in adult primary visual cortex. Nature 356, 150–152.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Graham, J., Lin, C.-S. & Kaas, J.H. (1979). Subcortical projections of six visual cortical areas in the owl monkey, Aotus trivirgatus. Journal of Comparative Neurology 187, 557–580.CrossRefGoogle ScholarPubMed
Hassler, R. (1967). Comparative anatomy of central visual systems in day- and night-active primates. In Evolution of the Forebrain, ed. Hassler, R. & Stephan, H., pp. 419–434. New York: Plenum Press.Google Scholar
Heinen, S.J. & Skavenski, A.A. (1991). Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey. Experimental Brain Research 83, 670–674.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. Journal of Comparative Neurology 182, 123–136.CrossRefGoogle Scholar
Henry, G.H. (1991). Afferent inputs, receptive-field properties and morphological cell types in different laminae of the striate cortex. In Vision and Vision Dysfunction, The Neural Basis of Vision Function, ed. Leventhal, A.G., pp. 223–245. London: McMillan Press Ltd.Google Scholar
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
Hubel, D.H., Weisel, T.N. & LeVay, S. (1977). Plasticity of ocular-dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society 278, 377–409.Google ScholarPubMed
Humphrey, A.L., Sur, M., Uhlrich, D.J. & Sherman, S.M. (1985). Projection pattern of individual x- and y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat. Journal of Comparative Neurology 233, 159–189.CrossRefGoogle ScholarPubMed
Kaas, J.H. (1986). The structural basis for information processing in the primate visual system. In Visual Neuroscience, ed. Pettigrew, K. & Sanderson, J., pp. 315–340. Cambridge, England: Cambridge University Press.Google Scholar
Kaas, J.H. (1991). Plasticity of sensory and motor maps in adult mammals. Annual Review of Neuroscience 14, 137–167.CrossRefGoogle ScholarPubMed
Kaas, J.H., Lin, C.-S. & Casagrande, V.A. (1976). The relay of ipsi-lateral and contralateral retinal inputs from the lateral geniculate nucleus to striate cortex in owl monkey: A transneuronal transport study. Brain Research 106, 371–378.CrossRefGoogle 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 of primates. Journal of Comparative Neurology 182, 517–554.CrossRefGoogle ScholarPubMed
Kaas, J.H., Krubitzer, L.A., Chino, Y.M., Langston, A.L., Polley, E.H. & Blair, N. (1990). Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229–231.CrossRefGoogle ScholarPubMed
Krubitzer, L.A. & Kaas, J.H. (1990). Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns. Visual Neuroscience 5, 165–204.CrossRefGoogle ScholarPubMed
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceedings of the National Academy of Sciences of the U.S.A. 89, 3566–3570.CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1988). Development of primate retinogeniculate axon arbors. Visual Neuroscience 1, 103–123.CrossRefGoogle ScholarPubMed
LeVay, S. & Stryker, 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 for Neurosciences.Google Scholar
LeVay, S., Stryker, M.P. & Schatz, 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.CrossRefGoogle ScholarPubMed
LeVay, S., Weisel, 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
Lin, C.-S. & Kaas, J.H. (1977). Projections from cortical visual areas 17, 18, and MT onto the dorsal lateral geniculate nucleus in owl monkeys. Journal of Comparative Neurology 173, 457–473.CrossRefGoogle ScholarPubMed
Lin, C.-S. & Kaas, J.H. (1979). The inferior pulvinar complex in owl monkeys: Architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex. Journal of Comparative Neurology 187, 655–678.CrossRefGoogle ScholarPubMed
Lin, C.-S. & Kaas, J.H. (1980). Effects of monocular deprivation on geniculocortical pathways in the owl monkey. Neuroscience Letters 18, 267–273.CrossRefGoogle ScholarPubMed
Lin, C.-S., Weller, R.E. & Kaas, J.H. (1982). Cortical connections of striate cortex in the owl monkey. Journal of Comparative Neurology 211, 165–176.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate cortex. Annual Review in Neuroscience 11, 253–288.CrossRefGoogle Scholar
Lund, J.S., Hawken, M.J. & Parker, A.J. (1988). Local circuit neurons of macaque monkey striate cortex: II. Neurons of laminae 5B and 6. Journal of Comparative Neurology 276, 1–29.CrossRefGoogle ScholarPubMed
Lund, J.S. & Holbach, S.M. (1991). Postnatal development of thalamic recipient neurons in the monkey striate cortex: Comparison of spine acquisition and dendritic growth of layer 4C alpha and beta spiny stellate neurons. Journal of Comparative Neurology 309, 115–128.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Pospichal, M.W., Florence, S.L. & Kaas, J.H. (1992). The postnatal development of M cell axon arbors in primary visual cortex of monkeys. Investigations in Ophthalmology and Visual Science (Suppl.) 33, 2613.Google Scholar
Pospichal, M.W., Florence, S.L. & Kaas, J.H. (1993). The postnatal development of geniculocortical axon arbors in monkeys. Investigations in Ophthalmology and Visual Science (Suppl.) 34, 2186.Google Scholar
Purves, D. & LaMantia, A.S. (1990). Numbers of “blobs” in the primary visual cortex of neonatal and adult monkeys. Proceedings of the National Academy of Sciences of the U.S.A. 87, 5764–5767.CrossRefGoogle ScholarPubMed
Raczkowski, D. & Fitzpatrick, D. (1990). Terminal arbors of individual, physiologically identified geniculocortical axons in the tree shrew’s striate cortex. Journal of Comparative Neurology 302, 500–514.CrossRefGoogle ScholarPubMed
Rakic, P. (1977). Prenatal development of the visual system in the rhesus monkey. Philosophical Transactions of the Royal Society (London) 278, 245–260.Google ScholarPubMed
Rockland, K.S. & Virga, A. (1990). Organization of individual cortical axons projecting from area V1 (area 17) to V2 (area 18) in the macaque monkey. Visual Neuroscience 4, 11–28.CrossRefGoogle ScholarPubMed
Rowe, M.H., Benevento, L.A. & Rezak, M. (1978). Some observations on the patterns of segregated geniculate inputs to the visual cortex in New World primates: An autoradiographic study. Brain Research 159, 371–378.CrossRefGoogle Scholar
Sherman, S.M., Wilson, J.R., Kaas, J.H. & Webb, S.V. (1976). X-and y-cells of the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). Science 192, 475–477.CrossRefGoogle ScholarPubMed
Spatz, W.B. & Tigges, J. (1972). Experimental-anatomical studies on the “middle temporal visual area (MT)” in primates: I. Efferent cortico-cortical connections in the marmoset, Callithrix jacchus. Journal of Comparative Neurology 146, 451–461.CrossRefGoogle ScholarPubMed
Stone, J. (1983). Parallel Processing in the Visual System, New York: Plenum Press, pp. 438.CrossRefGoogle Scholar
Tigges, J., Tigges, M., Anschel, S., Cross, N.A., Letbetter, W.D. & McBride, R.L. (1981). Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19, and MT in the squirrel monkey (Saimiri). Journal of Comparative Neurology 202, 539–560.CrossRefGoogle ScholarPubMed
Tootell, R.B., Hamilton, S.L. & Silverman, M.S. (1985). Topography of cytochrome oxidase activity in owl monkey cortex. Journal of Neuroscience 5, 2786–2800.CrossRefGoogle ScholarPubMed
Usrey, W.M., Muly, E.C & Fitzpatrick, D. (1992). Lateral geniculate projections to the superficial layers of visual cortex in the tree shrew. Journal of Comparative Neurology 319, 159–171.CrossRefGoogle Scholar
Van Essen, D.C. (1985). Functional organization of primate visual cortex. In Central Cortex, ed. Peters, A. & Jones, E.G., pp. 259–329. New York: Plenum Press.Google Scholar
Walker, E.P. (1964). Mammals of the World, Vol. I, p. 426. Baltimore, Maryland: Johns Hopkins Press.Google Scholar
Weber, J.T, Huerta, M.F., Kaas, J.H. & Harting, J.K. (1983). The projections of the lateral geniculate nucleus of the squirrel monkey: Studies of the interlaminar zones and the S layers. Journal of Comparative Neurology 213, 135–145.CrossRefGoogle ScholarPubMed
Weller, R.E. & Kaas, J.H. (1987). Subdivisions and connections of inferior temporal cortex in owl monkeys. Journal of Comparative Neurology 256, 137–172.CrossRefGoogle ScholarPubMed
Weller, R.E., Wall, J.T. & Kaas, J.H. (1984). Cortical connections of the middle temporal visual (MT) and superior temporal cortex in owl monkeys. Journal of Comparative Neurology 288, 81–104.CrossRefGoogle Scholar