Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-24T00:34:55.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Development of the visual callosal cell distribution in the rat: Mature features are present at birth

Published online by Cambridge University Press:  02 June 2009

Cynthia S. Hernit ,
Kathryn M. Murphy  and
Richard C. van Sluyters
Cynthia S. Hernit
Affiliation:
Department of Molecular and Cell Biology, University of California, Berkeley
Kathryn M. Murphy
Affiliation:
Department of Psychology, McMaster University, 1280 Main St. W., Hamilton, Ontario
Richard C. van Sluyters
Affiliation:
School of Optometry, University of California, Berkeley
Get access Rights & Permissions [Opens in a new window]

Abstract

In the present study, the early postnatal distribution and subsequent fate of visual callosal neurons were studied in neonatal rat pups. Previous studies had indicated that the adult pattern of visual callosal neurons was sculpted from an initially uniform distribution in the neonatal cortex. To reexamine this issue, we used a sensitive tracer, latex microspheres conjugated either to rhodamine or fluorescein, that was injected into the occipital cortex of one hemisphere in pups on the day of birth (PND 1), PND 6, or PND 12. Examination of the resulting retrograde labeling of cortical neurons in the opposite hemisphere indicates that features of the mature visual callosal pattern are present as early as PND 1. At all stages of postnatal development, the relative density of callosal projection cells varies consistently across the mediolateral extent of primary visual cortex —it is always highest in the region of the 17/18a border and lowest in the body of area 17. These data strongly suggest that, from the outset, visual cortical neurons in the region of the 17/18a border preferentially make connections with the opposite hemisphere. The results of experiments in which callosal neurons were labeled on the day of birth indicate that only those neurons that have migrated to their final cortical destinations have extended callosal axons into the vicinity of the visual cortex in the opposite hemisphere. The initial pattern of callosal neurons resembles a dense, compact version of the mature one, and the present study suggests that much of the remaining change in the appearance of this pathway may be accounted for by the decrease in the overall density of neurons that is due to expansion of the cortical gray matter during postnatal life. Taken together, these results suggest that the development of the visual callosal pathway in the rat may be more similar to that in the monkey than has been reported previously.

Keywords

Corpus callosumInterhemispheric pathwaysDevelopmentVisual cortex
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 5 , September 1996 , pp. 923 - 943
Copyright
Copyright © Cambridge University Press 1996

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

Bentivoglio, M., Kuypers, H.G.J.M., Catsman-Berrevoets, C.E., Loewe, H. & Dann, O. (1980). Two new fluorescent neuronal tracers which are transported over long distances. Neuroscience Letters 18, 25–30.Google Scholar
Berry, M. & Rogers, A.W. (1965). The migration of neuroblasts in the developing cerebral cortex. Journal of Anatomy 99, 691–709.Google Scholar
Butcher, L.L., Talbot, K. & Biletzikjian, L. (1975). Acetylcholin-esterase neurons in dopamine containing regions of the brain. Journal of Neural Transmission 37, 127–153.CrossRefGoogle Scholar
Catalano, S.M., Robertson, R.T. & Killackey, H.P. (1991). Early ingrowth of thatamocortical afferents to the neocortex of the prenatal rat. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2999–3003.Google Scholar
Caviness, V.S. Jr., (1975). Architectonic map of neocortex of the normal mouse. Journal of Comparative Neurology 164, 247–264.Google Scholar
Chalupa, L.M., Killackey, H.P., Snider, C.J. & Lia, B. (1989). Callosal projection neurons in area 17 of the fetal rhesus monkey. Developmental Brain Research 46, 303–308.CrossRefGoogle ScholarPubMed
Chalupa, L.M. & Killackey, H.P. (1989). Process elimination underlies ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey. Proceedings of the National Academy of Sciences of the U.S.A. 6, 1076–1079.CrossRefGoogle Scholar
Cipolloni, P.B. & Peters, A. (1979). The bilaminar and banded distribution of the callosal terminals in the posterior neocortex of the rat. Brain Research 176, 33–47.Google Scholar
Connors, B.W., Benardo, L.S. & Prince, D.A. (1983). Coupling between neurons of the developing rat neocortex. Journal of Neuroscience 3, 773–782.Google Scholar
Cusick, C.G. & Lund, R.D. (1981). The distribution of the callosal projection to the occipital visual cortex in rats and mice. Brain Research 214, 239–259.CrossRefGoogle Scholar
Cusick, C.G. & Lund, R.D. (1982). Modification of visual callosal projections in rats. Journal of Comparative Neurology 212, 385–398.CrossRefGoogle ScholarPubMed
Dehay, C., Kennedy, H., Bullier, J. & Berland, M. (1988). Absence of interhemispheric connections of area 17 during development in the monkey. Nature 331, 348–350.CrossRefGoogle ScholarPubMed
Finlay, B.L. & Slattery, M. (1983). Local differences in the amount of early cell death in neocortex predict adult local specialization. Science 219, 1349–1351.Google Scholar
Friauf, E., McConnell, S.K. & Shatz, C.J. (1990). Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. Journal of Neuroscience 10, 2601–2613.Google Scholar
Gravel, C., Sasseville, R. & Hawkes, R. (1990). Maturation of the corpus callosum of the rat: II. Influence of thyroid hormones on the number and maturation of axons. Journal of Comparative Neurology 291, 147–161.Google Scholar
Heaton, M.B., Moody, S.A. & Kosier, M.E. (1978). Peripheral innervation by migrating neuroblasts in the chick embryo. Neuroscience Letters 10, 55–59.Google Scholar
Hernit, C.S., Murphy, K.M. & Van Sluyters, R.C. (1989). The development of callosal cell distribution in the visual cortex of neonatal rats. Society for Neuroscience Abstracts 15, 1338.Google Scholar
Hernit, C.S., Van Sluyters, R.C. & Murphy, K.M. (1990). Visual callosal development in neonatal rats: Do migrating or undifferentiated cells have an interhemispheric axon? Society for Neuroscience Abstracts 16, 803.Google Scholar
Heumann, D., Leuba, G. & Rabinowicz, T. (1977). Postnatal development of the mouse cerebral neocortex II. Quantitative cytoarchitectonics of visual and auditory areas. Journal fur Hirnforschung 18, 483–500.Google ScholarPubMed
Hicks, S.P. & D'Amato, C.J. (1968). Cell migrations to the isocortex in the rat. Anatomical Record 160, 619–634.Google Scholar
Hogan, D. & Herman, N.E.J. (1990). Growth cone morphology, axon trajectory and branching patterns in the neonatal rat corpus callosum. Developmental Brain Research 53, 283–287.CrossRefGoogle ScholarPubMed
Innocenti, G.M. (1981). Growth and reshaping of axons in the establishment of visual callosal connections. Science 212, 824–827.Google Scholar
Innocenti, G.M. & Caminiti, R. (1980). Postnatal shaping of callosal connections from sensory areas. Experimental Brain Research 38, 381–394.CrossRefGoogle ScholarPubMed
Innocenti, G.M., Fiore, L. & Caminiti, R. (1977). Exuberant projection into the corpus callosum from the visual cortex of newborn cats. Neuroscience Letters 4, 237–242.CrossRefGoogle ScholarPubMed
Ivy, G.O., Akers, R.M. & Killackey, H.P. (1979). Differential distribution of callosal projection neurons in the neonatal and adult rat. Brain Research 173, 532–537.Google Scholar
Ivy, G.O. & Killackey, H.P. (1981). The ontogeny of the distribution of callosal projection neurons in the rat parietal cortex. Journal of Comparative Neurology 195, 367–389.Google Scholar
Ivy, G.O. & Killackey, H.P. (1982). Ontogenetic changes in the projections of neocortical neurons. Journal of Neuroscience 2, 735–743.Google Scholar
Katz, L.C., Burkhalter, A. & Dreyer, W.J. (1984). Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310, 498–500.CrossRefGoogle ScholarPubMed
Katz, L.C. & Iarovici, D.M. (1990). Green fluorescent latex micro-spheres: A new retrograde tracer. Neuroscience 34, 511–520.Google Scholar
Koralek, K. & Killackey, H.P. (1990). Callosal projections in rat somatosensory cortex are altered by early removal of afferent input. Proceedings of the National Academy of Sciences of the U.S.A. 87, 1396–1400.Google Scholar
Krieg, W.J.S. (1946). Connections of the cerebral cortex. I. The albino rat. B. Structure of the cortical areas. Journal of Comparative Neurology 84, 277–324.Google Scholar
LaMantia, A.-S. & Rakic, P. (1990). Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey. Journal of Neuroscience 10, 2156–2175.Google Scholar
Levi-Montalcini, R. (1950). The origin and development of the visceral system in the spinal cord of the chick embryo. Journal of Morphology 86, 253–284.Google Scholar
Lo Turco, J.J. & Kriegstein, A.R. (1991). Clusters of coupled neuroblasts in embryonic neocortex. Science 252, 563–566.Google Scholar
Lund, R.D., Chang, F.-L.F. & Land, P.W. (1984). The development of callosal projections in normal and one-eyed rats. Brain Research 14, 139–142.Google Scholar
Lund, R.D. & Mustari, M.J. (1977). Development of the geniculocortical pathway in rats. Journal of Comparative Neurology 173, 289–306.Google Scholar
Luskin, M.B. & Shatz, C.J. (1985). Neurogenesis of the cat's primary visual cortex. Journal of Comparative Neurology 242, 611–631.Google Scholar
Marin-Padilla, M. (1978). Dual origin of the mammalian neocortex and evolution of the cortical plate. Anatomy and Embryology 152, 109–126.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.Google Scholar
McConnell, S.K. & Kaznowski, C.E. (1991). Cell cycle dependence of laminar determination in developing neocortex. Science 254, 282–285.Google Scholar
Meissirel, C., Dehay, D., Berland, M. & Kennedy, H. (1991). Segregation of callosal and association pathways during development in the visual cortex of the primate. Journal of Neuroscience 11, 3297–3316.CrossRefGoogle ScholarPubMed
Miller, M.W. (1986). The migration and neurochemical differentiation of γ-aminobutyric acid (GABA)-immunoreactive neurons in rat visual cortex as demonstrated by a combined immunocytochemical-autoradiographic technique. Developmental Brain Research 28, 41–46.Google Scholar
Miller, M.W. (1988). Development of projection and local circuit neurons in neocortex. In Cerebral Cortex, ed. Peters, A. & Jones, E.G., pp. 133–175. New York: Plenum Publishing Corp.Google Scholar
Miller, M.W. & Nowakowski, R.S. (1988). Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system. Brain Research 457, 44–52.Google Scholar
Miller, M.W. & Vogt, B.A. (1984 a). The postnatal growth of the callosal connections of primary and secondary visual cortex in the rat. Developmental Brain Research 14, 304–309.Google Scholar
Miller, M.W. & Vogt, B.A. (1984 b). Heterotopic and homotopic callosal connections in rat visual cortex. Brain Research 297, 75–89.CrossRefGoogle ScholarPubMed
Morris, C.R. & Kalil, K. (1991). Guidance of callosal axons by radial glia in the developing cortex. Journal of Neuroscience 11, 3481–3492.Google Scholar
Olavarria, J. & Van Sluyters, R.C. (1983). Widespread callosal connections in infragranular visual cortex of the rat. Brain Research 279, 233–237.Google Scholar
Olavarria, J. & Van Sluyters, R.C. (1985). Organization and postnatal development of callosal connections in the visual cortex of the rat. Journal of Comparative Neurology 239, 1–26.Google Scholar
Olavarria, J., Malach, R. & Van Sluyters, R.C. (1987). Development of visual callosal connections in neonatally enucleated rats. Journal of Comparative Neurology 260, 321–348.Google Scholar
O'Leary, D.D.M., Stanfield, B. & Cowan, W.M. (1981). Evidence that the early postnatal restriction of the cells of origin of the corpus callosal projections is due to the elimination of axon collaterals rather than to the death of neurons. Developmental Brain Research 25, 607–617.Google Scholar
Parnavelas, J.G., Barfield, J.A., Franke, E. & Luskin, M.B. (1991). Separate progenitor cells give rise to pyramidal and nonpyramidal neurons in the rat telencephalon. Cerebral Cortex 1, 463–468.CrossRefGoogle ScholarPubMed
Peinado, A., Yuste, R. & Katz, L.C., (1993). Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10, 103–114.Google Scholar
Peters, A., Feldman, M.L. & Vaughan, D.W. (1983). The effect of aging on the neuronal population within area 17 of adult rat cerebral cortex. Neurobiology of Aging 4, 273–282.Google Scholar
Rakic, P. (1977). Prenatal development of the visual system in rhesus monkey. Philosophical Transactions of the Royal Society B (London) 278, 245–260.Google ScholarPubMed
Reinoso, B.S. & O'Leary, D.D.M. (1990). Correlation of geniculocor-tical growth into the cortical plate with the migration of their layer IV and VI target cells. Society for Neuroscience Abstracts 16, 493.Google Scholar
Rhoades, R.W. & Dellacroce, D.D. (1980). Neonatal enucleation induces an asymmetric pattern of visual callosal connections in hamsters. Brain Research 202, 189–195.Google Scholar
Rhoades, R.W., Fish, S.E., Mooney, R.D. & Chiaia, N.L. (1987). Distribution of visual callosal projection neurons in hamsters subjected to transection of the optic radiation on the day of birth. Developmental Brain Research 32, 217–232.Google Scholar
Robertson, R.T. (1987). A morphogenetic role for transiently expressed AChE in developing thalamocortical systems? Neuroscience Letters 75, 259–264.Google Scholar
Robertson, R.T., Tijerina, A.A. & Gallivan, M.E. (1985). Transient patterns of acetylcholinesterase activity in visual cortex of rat: Normal development and the effects of neonatal monocular enucleation. Developmental Brain Research 21, 203–214.Google Scholar
Rothblat, L.R. & Hayes, L. (1982). Age-related changes in the distribution of visual callosal neurons following monocular enucleation in the rat. Brain Research 246, 145–149.Google Scholar
Schreyer, D.J. & Jones, E.G. (1982). Growth and target finding by axons of the corticospinal tract in prenatal and postnatal rats. Neuroscience 7, 1837–1853.Google Scholar
Schwartz, M.L., Rakic, P. & Goldman-Rakic, P.S. (1991). Early phenotype expression of cortical neurons: Evidence that a subclass of migrating neurons have callosal axons. Proceedings of the National Academy of Sciences of the U.S.A. 88, 1354–1358.Google Scholar
Shatz, C.J., Chun, J.J.M. & Luskin, M.B. (1988). The role of the subplate in the development of the mammalian telencephalon. In Cerebral Cortex, ed. Peters, A. & Jones, E.G., pp. 35–58. New York: Plenum Publishing.Google 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.Google Scholar
Shmued, L.C. & Fallon, J.H. (1986). Fluoro-Gold: A new fluorescent retrograde axonal tracer with numerous unique properties. Brain Research 377, 147–154.Google Scholar
Shoukimas, G.M. & Hinds, J.W. (1978). The development of the cerebral cortex in the embryonic mouse: An electronic microscopic serial section analysis. Journal of Comparative Neurology 179, 795–830.Google Scholar
Wise, S.P., Hendry, S.H.C. & Jones, E.G. (1977). Prenatal development of sensorimotor cortical projections in cats. Brain Research 138, 538–544.Google Scholar
Wise, S.P. & Jones, E.G. (1976). The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. Journal of Comparative Neurology 168, 313–344.Google Scholar
Yuste, R., Peinado, A. & Katz, L.C. (1992). Neuronal domains in developing neocortex. Science 257, 665–669.Google Scholar