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Generation of Cell Diversity in the Mammalian Visual Cortex

  • Chapter
The Visual System from Genesis to Maturity

Abstract

One of the hallmarks of the central nervous system (CNS) of all mammalian species is that it contains a diverse population of specialized cell types and specific sets of connections. The cerebral cortex is the ultimate example of such specificity where a unique pattern of afferent and efferent connections distinguish a large number of individual cortical areas, each containing a heterogeneous array of neuronal and glial subtypes. The visual cortex, the topic of this chapter, is one such area. To ensure the emergence of such complexity, the developing nervous system has somehow devised a way to regulate the number of cells generated, their distribution, their course of differentiation, and the connections they form. This chapter is concerned with a consideration of how the immense variety of cells belonging to the cerebral cortex, and visual cortex in particular, arises during the course of development. Any acceptable explanation of how cells acquire their identity must account for the observation that all of the cells of the cerebral cortex—both neurons and glia—are derived from a seemingly homogeneous layer of neuroepithelial cells surrounding the immature cerebral ventricles, known as the ventricular zone. The question this raises is whether the cells of the ventricular zone form a homogeneous population, or whether it might contain distinct sets of progenitor cells that give rise exclusively to one type of cell: either all neurons, all astrocytes, or all oligodendrocytes. This also raises the related question of if and when lineage restrictions occur among the population of progenitor cells producing the cells of the mature cerebral cortex. An analysis of the phenotype of the progeny of individual progenitor cells of the ventricular zone would shed light on these questions. As will be discussed below, the adaptation of recombinant retroviruses as tools to study cell lineage has placed such an analysis of the genealogical relationships of cells of the cerebral cortex within the realm of possibility.

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References

  • Anderson DJ (1989): The neural crest cell lineage problem: Neuropoiesis? Neuron 3:1–12.

    Article  Google Scholar 

  • Angevine JB, Sidman RL (1961): Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766–768.

    Article  Google Scholar 

  • Austin CP, Cepko CL (1990): Cellular migration patterns in the developing mouse cerebral cortex. Development 110:713–732.

    Google Scholar 

  • Banerjee U, Zipursky SL (1990): The role of cell-cell interaction in the development of the Drosophila visual system. Neuron 4:177–187.

    Article  Google Scholar 

  • Barfield JA, Parnavelas JG, Luskin MB (1990): Separate progenitor cells give rise to neurons, astrocytes and oligodendrocytes in the rat cerebral cortex. Neurosci Abstr 16:1272.

    Google Scholar 

  • Baughman RW, Gilbert CD (1981): Aspartate and glutamate as possible neurotransmitters in the visual cortex. J Neurosci 1:427–439.

    Google Scholar 

  • Berry M, Rogers AW (1965): The migration of neuroblasts in the developing cerebral cortex. J Anat 99:691–709.

    Google Scholar 

  • Bunge MB, Wood PM, Tynar LB, Bates ML, Sanes JR (1989): Perineurium originates from fibroblasts: Demonstration in vitro with a retroviral marker. Science 243: 229–231.

    Article  Google Scholar 

  • Caviness VS, Jr (1982): Neocortical histogenesis in normal and Reeler mice: A development study based upon 3H-thymidine autoradiography. Dev Brain Res 4:293–302.

    Article  Google Scholar 

  • Caviness VS. Jr, Sidman RL (1973): Time of origin of corresponding cell classes in the cerebral cortex of normal and Reeler mutant mice: An autoradiographic analysis. J Comp Neurol 148:141–151.

    Article  Google Scholar 

  • Colonnier M (1981): The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In: The Organization of the Cerebral Cortex, Schmitt FO, Worden FG, Adelman G, Dennis SG, eds. Cambridge: MIT Press.

    Google Scholar 

  • Conti F, Rustioni A, Petrusz P, Towle AC (1987): Glutamate-positive neurons in the somatic sensory cortex of rats and monkeys. J Neurosci 7:1887–1901.

    Google Scholar 

  • Doupe AJ, Landis SC, Patterson PH (1985): Environmental influences in the development of neural crest derivatives: Glucocorticoids, growth factors, and chromaffin cell plasticity. J Neurosci 5:2119–2142.

    Google Scholar 

  • Fairen A, Cobas A, Fonseca M (1986): Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex. J Comp Neurol 251:67–83.

    Article  Google Scholar 

  • Galileo DS, Gray GE, Owens GC, Majors J, Sanes JR (1990): Neurons and glia arise from a common progenitor in chick optic tectum: demonstration with two retroviruses and cell-type specific antibodies. PNAS 87:458–462.

    Article  Google Scholar 

  • Gilbert CP (1983): Neurocircuitry of the visual cortex. Ann Rev Neurosci 6:217–247.

    Article  Google Scholar 

  • Hendry SHC, Jones EG (1986): Reduction in number of immunostained GABAergic neurons in deprived-eye dominance columns of monkey area 17. Nature 320:750–753.

    Article  Google Scholar 

  • His W (1889): Die neuroblasten und deren Entstehung im embryonalen. Marke Abn Phys Cl Kgl Sach ges Wiss 15:313–372.

    Google Scholar 

  • Houser CR, Hendry SHC, Jones EG, Vaughn JE (1983): Morphological diversity of immunocytochemically identified GABA neurons in the monkey sensory-motor cortex. J Neurocytol 12:617–638.

    Article  Google Scholar 

  • Ichikawa M, Hirata Y (1982): Morphology and distribution of postnatally generated glial cells in the somatosensory cortex of the rat: An autoradiographic and electron microscopic study. Dev Brain Res 4:369–377.

    Article  Google Scholar 

  • Jones EG, Hendry SHC (1986): Peptide containing neurons in primate cerebral cortex. In: Neuropeptides in Neurologic and Psychiatric Diseases, Martin JB, Barchas JD, eds. New York: Raven Press.

    Google Scholar 

  • Jones EG, Powell TPS (1970): Electron microscopy of the somatic sensory cortex of the cat: 1. Cell types and synaptic organization. Philos Trans R Soc Lond (Biol) 257:1–11.

    Article  Google Scholar 

  • Kenyon C (1985): Cell lineage and the control of Caenorhabditis elegans development. Philos Trans R Soc Lond (Biol) 312:21–38.

    Article  Google Scholar 

  • LeVine SM, Goldman JE (1988a): Embryonic divergence of oligodendrocyte and astrocyte lineages in developing rat cerebrum. J Neurosci 8:3992–4006.

    Google Scholar 

  • LeVine SM, Goldman JE (1988b): Spatial and temporal patterns of oligodendrocyte differentiation in rat cerebrum and cerebellum. J Comp Neurol 277:441–455.

    Article  Google Scholar 

  • Levitt P, Cooper ML, Rakic P (1981): Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: An ultrastructural immunoperoxidase analysis. J Neurosci 1:27–39.

    Google Scholar 

  • Levitt P, Cooper ML, Rakic P (1983): Early divergence and changing proportions of neuronal and glial precursor cells in the primate cerebral ventricular zone. Dev Biol 96:472–484.

    Article  Google Scholar 

  • Lin C-S, Lu SM, Schmechel DE (1986): Glutamic acid decarboxylase and somatostatin immunoreactivities in rat cerebral cortex. J Comp Neurol 244:369–383.

    Article  Google Scholar 

  • Luskin MB (1990): Generation of cell diversity in the cerebral cortex: Lineage relationships. Eur Neurosci Assoc Abstr 22:4.

    Google Scholar 

  • Luskin MB, Parnavelas JG, Barfield TA: Neurons, astrocytes and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: on ultrastructural analysis of clonally related cells, (submitted).

    Google Scholar 

  • Luskin MB, Pearlman A, Sanes JR (1988): Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1:635–647.

    Article  Google Scholar 

  • Luskin MB, Shatz CJ (1985): Pattern of neurogenesis of the cat’s primary visual cortex. J Comp Neurol 242:611–631.

    Article  Google Scholar 

  • Mares V, Bruckner G (1978): Postnatal formation of non-neuronal cells in the rat occipital cerebrum: An autoradiographic study of the time and space pattern of cell division. J Comp Neurol 177:519–528.

    Article  Google Scholar 

  • McConnell SK (1988): Development and decision-making in the mammalian cerebral cortex. Brain Res Rev 13:1–23.

    Article  Google Scholar 

  • McConnell SK, Kaznowski CE (1991): Cell cycle dependence of laminar determination in developing neocortex. Science 254:282–285.

    Article  Google Scholar 

  • Meiler K, Tetzlaff W (1975): Neuronal migration during the early development of the cerebral cortex: A scanning electron microscope study. Cell Tissue Res 163:313–325.

    Google Scholar 

  • Meyer G, Wahle P (1988): Early postnatal development of cholecystokinin-immunoreactive structures in the visual cortex of the cat. J Comp Neurol 276:360–386.

    Article  Google Scholar 

  • Miller MW (1985): Cogeneration of retrogradely labeled corticocortical projection and GABA-immunoreactive local circuit neurons in cerebral cortex. Dev Brain Res 23:187–192.

    Article  Google Scholar 

  • Miller MW (1986): The migration and neurochemical differentiation of gamma-aminobutyric acid (GABA)-immunoreactive neurons in rat visual cortex as demonstrated by a combined immunocytochemical-autoradiographic technique. Dev Brain Res 28: 41–46.

    Article  Google Scholar 

  • Miller RH, ffrench-Constant C, Raff MC (1989): The macroglial cells of the rat optic nerve. Ann Rev Neurosci 12:517–34.

    Article  Google Scholar 

  • Misson J-P, Austin CP, Takahashi T, Cepko C, Caviness VS Jr (1991): The alignment of migrating neural cells in relation to the murine neopallial radial glial fiber system. Cerebral Cortex 1:221–229.

    Article  Google Scholar 

  • Misson J-P, Edwards MA, Yamamoto M, Caviness VS Jr (1988): Identification of radial glial cells within the developing murine central nervous system: Studies based upon a new immunohistochemical marker. Dev Brain Res 44:95–108.

    Article  Google Scholar 

  • Naegele JR, Arimatsu Y, Schwartz P, Barnstable CJ (1988): Selective staining of a subset of GABAergic neurons in cat visual cortex by monoclonal antibody VC1.1. J Neurosci 8:79–89.

    Google Scholar 

  • Parnavelas JG, Barfield JA, Frank E, Luskin MB (1991): Separate progenitor cells give rise to pyramidal and nonpyramidal neurons in the rat telencephalon. Cerebral Cortex 1:463–468.

    Article  Google Scholar 

  • Parnavelas JG, Barfield JA, Luskin MB (1990): Lineage relationships of pyramidal and nonpyramidal neurons in the rat cerebral cortex. Neurosci Abstr 16:1272.

    Google Scholar 

  • Parnavelas JG, Dinopoulos A, Davies SW (1989): The central visual pathways. In: Handbook of Chemical Neuroanatomy, vol. 7, Integrated systems of the CWS, Pt II (Bjorklund A, Hokfelt T, Swanson SW, eds), pp 1–164. Amsterdam: Elsevier.

    Google Scholar 

  • Parnavelas JG, Papadopoulos GC, Cavanagh ME (1988): Changes in neurotransmitters during development. In: Cerebral Cortex, vol. 7, Jones EG, Peters A, eds. New York: Plenum Press.

    Google Scholar 

  • Parnavelas JG, Sullivan K, Lieberman AR, Webster KE (1977): Neurons and their synaptic organization in the visual cortex of the rat: Electron microscopy of Golgi preparations. Cell Tissue Res 183:499–517.

    Article  Google Scholar 

  • Patterson PH (1978): Environmental determination of autonomie neurotransmitter functions. Ann Rev Neurosci 1:1–17.

    Article  Google Scholar 

  • Peters A (1985): The visual cortex of the rat. In: Cerebral Cortex, vol. 3, Jones EG, Peters A, eds. New York: Plenum Press.

    Google Scholar 

  • Peters A, Feldman M (1973): The cortical plate and molecular layer of the late rat fetus. Z Anat Entwickl-Gesch 141:3–37.

    Article  Google Scholar 

  • Peters A, Palay SL, Webster de F (1976): The Fine Structure of the Nervous System. Philadelphia: Saunders.

    Google Scholar 

  • Potter DD, Landis SC, Matsumoto SG, Furshpan EJ (1986): Synaptic functions in rat sympathetic neurons in microcultures: 2. Adrenergic/cholinergic dual status and plasticity. J Neurosci 6:1080–1098.

    Google Scholar 

  • Price J, Thurlow L (1988): Cell lineage in the rat cerebral cortex: A study using retroviral-mediated gene transfer. Development 104:473–482.

    Google Scholar 

  • Price JL, Turner D, Cepko C (1987): Lineage analysis in the vertebrate nervous system by retrovirus mediated gene transfer. PNAS USA 84:156–160.

    Article  Google Scholar 

  • Privat A (1975): Postnatal gliogenesis in the mammalian brain. Int Rev Cytol 40:281–323.

    Article  Google Scholar 

  • Raedler E, Raedler A (1978): Autoradiographic study of early neurogenesis in rat neocortex. Anat Embryol (Berl) 154:267–284.

    Article  Google Scholar 

  • Raff MC (1989): Glial cell diversification in the rat optic nerve. Science 243:1450–1455.

    Article  Google Scholar 

  • Rakic P (1972): Mode of cell migration to the superficial layers of monkey neocortex. J Comp Neurol 145:61–84.

    Article  Google Scholar 

  • Rakic P (1974): Neurons in the rhesus monkey visual cortex: Systematic relation between time of origin and eventual disposition. Science 183:425–427.

    Article  Google Scholar 

  • Rakic P (1988): Specification of cerebral cortical areas. Science 241:170–176.

    Article  Google Scholar 

  • Sanes JR (1989): Analyzing cell lineage with a recombinant retrovirus. Trends Neurosci 12:21–28.

    Article  Google Scholar 

  • Sanes JR, Rubenstein JLR, Nicolas J-F (1986): Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J 5:3133–3142.

    Google Scholar 

  • Sauer FC (1935): Mitosis in the neural tube. J Comp Neurol 62:377–405.

    Article  Google Scholar 

  • Schaper A (1897): The earliest differentiation in the central nervous system of vertebrates. Science 5:430–431.

    Google Scholar 

  • Shimada M, Langman J (1970): Cell proliferation, migration and differentiation in the cerebral cortex of the golden hamster. J Comp Neurol 139:227–244.

    Article  Google Scholar 

  • Sidman RL, Rakic P (1973): Neuronal migration, with special reference to the developing human brain: A review. Brain Res 62:1–35.

    Article  Google Scholar 

  • Skoff RB (1980): Neuroglia: A re-evaluation of their origin and development. Pathol Res Pract 168:279–300.

    Article  Google Scholar 

  • Streit P (1984): Glutamate and aspartate as transmitter candidates for systems of the cerebral cortex. In: Cerebral Cortex, vol. 2, Jones EG, Peters A, eds. New York: Plenum Press.

    Google Scholar 

  • Sulston J, Schierenberg E, White JG, Thomson JN (1983): The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119.

    Article  Google Scholar 

  • Temple S (1989): Division and differentiation of isolated CNS blast cells in microculture. Nature 340:471–473.

    Article  Google Scholar 

  • Turner D, Cepko C (1987): A common progenitor for neurons and glia persists in rat retina late in development. Nature 328:131–136.

    Article  Google Scholar 

  • Vaughan DW (1984): The structure of neuroglial cells. In: Cerebral Cortex, vol. 2, Jones EG, Peters A, eds. New York: Plenum Press.

    Google Scholar 

  • Vaysse PJ-J, Goldman JE (1990): A clonal analysis of glial lineages in neonatal forebrain development in vitro. Neuron 5:227–235.

    Article  Google Scholar 

  • Walsh C, Cepko CL (1988): Clonally related cortical cells show several migration patterns. Science 241:1342–1345.

    Article  Google Scholar 

  • Wise SP (1985): Co-localization of GABA and neuropeptides in the cerebral cortex. Trends Neurosci 8:92–95.

    Article  Google Scholar 

  • Wolff JR, Bottacher H, Zetzshe T, Oertel WH, Chronwall BM (1984): Development of GABAergic neurons in rat visual cortex as identified by glutamate decarboxylase-like immunoreactivity. Neurosci Lett 47:207–212.

    Article  Google Scholar 

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Authors
  1. Marla B. Luskin
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Editors and Affiliations

  1. Departamento de Neurobiologia, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, 21941, Rio de Janeiro, R.J., Brazil

    Roberto Lent

  2. Centro de Ciências de Saúde, Bloco G Cidade Universitária, 21941, Rio de Janeiro, R.J., Brazil

    Roberto Lent

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Luskin, M.B. (1992). Generation of Cell Diversity in the Mammalian Visual Cortex. In: Lent, R. (eds) The Visual System from Genesis to Maturity. Birkhäuser, Boston, MA. https://doi.org/10.1007/978-1-4899-6726-8_9

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  • DOI: https://doi.org/10.1007/978-1-4899-6726-8_9

  • Publisher Name: Birkhäuser, Boston, MA

  • Print ISBN: 978-1-4899-6728-2

  • Online ISBN: 978-1-4899-6726-8

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