Development of Cingulate Cortex: Proteins, Neurons, and afferents

  • Michael W. Miller
  • Richard T. Robertson

Abstract

During their development, neurons pass through various stages of ontogeny including neuronal proliferation, migration, differentiation, and death. Although the combined effects of the genetic and epigenetic factors shape the final neuronal product, the balance of these two factors apparently varies with the ontogenetic stage. For example, proliferating cells appear to be more affected by genetic factors than they are by epigenetic factors, whereas differentiating and dying neurons are more responsive to epigenetic factors.

Keywords

Migration Dopamine Serotonin Neurol Catecholamine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acklin SE, van der Kooy D (1991): Ventricular zone heterogeneity in the developing rat fore-brain. Soc Neurosci Abstr 17:1479Google Scholar
  2. Al-Ghoul WM, Miller MW (1989): Transient expression of Alz-50-immunoreactivity in developing rat neocortex: A marker for naturally occurring neuronal death? Brain Res 481:361–367Google Scholar
  3. Antonicek H, Persohn E, Schachner M (1987): Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration. J Cell Biol 104:1587–1595Google Scholar
  4. Audigier S, Barberis C (1985): Pharmacological characterization of two specific binding sites for neurohypophysial hormones in hippo-campal synaptic membranes of the rat. EMBO 7 4:665–685Google Scholar
  5. Austin CP, Cepko CF (1990): Cellular migration patterns in the developing mouse cerebral cortex. Development (Cambridge, UK) 110:713–732Google Scholar
  6. Barbe MF, Levitt P (1991): The early commitment of fetal neurons to the limbic cortex. J Neurosci 11:519–533Google Scholar
  7. Bayer SA (1985): Neurogenesis of the magnocel-lular basal telencephalic nuclei in the rat. Int J Dev Neurosci 3:229–243Google Scholar
  8. Bayer SA (1990): Neurogenetic patterns in the medial limbic cortex of the rat related to anatomical connections with the thalamus and striatum. Exp Neurol 107:132–142Google Scholar
  9. Bayer SA, Altman J (1991): Neocortical Development. New York: Raven PressGoogle Scholar
  10. Berger B, Verney C (1984): Development of the catecholamine innervation in rat neocortex: Morphological features. In: Monoamine Innervation of Cerebral Cortex. Descarries L, Reader TR, Jasper HH, eds. New York, Liss: pp 95–121Google Scholar
  11. Berger B, Verney C, Febvret A, Vigny A, Helle KB (1985): Postnatal ontogenesis of the dopaminergic innervation in the rat anterior cingu-late cortex (area 24). Immunocytochemical and catecholamine fluorescence histochemical analysis. Dev Brain Res 21:31–47Google Scholar
  12. Bigl V, Woolf NJ, Butcher LL (1982): Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital and cingu-late cortices: A combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 8:727–749Google Scholar
  13. Blue ME, Molliver ME (1987): 6-Hydroxy-dopamine induces serotonergic axon sprouting in cerebral cortex of newborn rat. Dev Brain Res 32:255–269Google Scholar
  14. Blue ME, Parnavelas JG (1982): The effect of neonatal 6-hydroxydopamine treatment on syn-aptogenesis in the visual cortex of the rat. J Comp Neurol 205:199–205Google Scholar
  15. Catalano SM, Robertson RT, Killackey HP (1991): Early ingrowth of thalamocortical Afferents to the neocortex of the prenatal rat. Proc Natl Acad Sci USA 88:2999–3003Google Scholar
  16. Clarke PGH (1985): Neuronal death in the development of the vertebrate nervous system. Trends Neurosci 8:345–349Google Scholar
  17. Cooper NGF, Steindler DA (1986): Lectins demarcate the barrel subfield in the somatosensory cortex of the early postnatal mouse. J Comp Neurol 249:57–169Google Scholar
  18. Cowan WM (1970): Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous system. In: Contemporary Research Methods in Neuroanatomy, Nauta WJH, Ebbesson SOE, eds. New York: Springer-Verlag, pp 217–251Google Scholar
  19. Coyle JT, Molliver ME (1977): Major innervation of newborn rat cortex by monoaminergic neurons. Science 196:444–447Google Scholar
  20. Cunningham TJ (1982): Naturally occurring death and its regulation by developing neural pathways. Int Rev Cytol 72:163–186Google Scholar
  21. D’Amato RJ, Blue ME, Largent B, Lynch DR, Ledbetter DJ, Molliver ME, Snyder SH (1987): Ontogeny of the serotonergic projection to rat neocortex: Transient expression of a dense innervation to primary sensory areas. Proc Natl Acad Sci USA 84:4322–4326Google Scholar
  22. Dinopoulos A, Eadie LA, Dori I, Parnavelas JG (1989): The development of basal forebrain projections to the rat visual cortex. Exp Brain Res 76:563–571Google Scholar
  23. Edelman GM (1987): Neural Darwinism. New York: Basic BooksGoogle Scholar
  24. Fernandez V (1969): An autoradiographic study of the development of the anterior thalamic group and limbic cortex in the rabbit. J Comp Neurol 136:423–452Google Scholar
  25. Finlay BL, Slattery M (1983): Local differences in the amount of early cell death in neocortex predict adult local specializations. Science 219:1349–1351Google Scholar
  26. Finlay BL, Wikler KC, Sengelaub DR (1987): Regressive events in brain development and scenarios for vertebrate brain evolution. Brain Behav Evol 30:102–117Google Scholar
  27. Foote SL, Morrison JH (1987): Development of the noradrenergic, serotonergic, and dopaminergic innervation of neocortex. Curr Top Dev 5/0/21:391–423Google Scholar
  28. Friedman WJ, Ernfors P, Persson H (1991): Transient and persistent expression of NT-3/HDNF mRNA in the rat brain during postnatal development. J Neurosci 11:1577–1584Google Scholar
  29. Gardette R, Courtois M, Bisconte J-C (1982): Prenatal development of mouse central nervous structures: Time of origin and gradients of neuronal production. A radioautographic study. J Hirnforsch 23:415–431Google Scholar
  30. Godement P, Vansslow J, Thanos S, Bonhoeffer F (1987): A study of developing visual systems with a new method for staining neurons and their processes in fixed tissue. Development (Cambridge, UK) 101:697–713Google Scholar
  31. Hamburger V, Levi-Montalcini R (1949): Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J Exp Zool 162:133–160Google Scholar
  32. Hamburger V, Oppenheim RW (1982): Naturally occurring neuronal death in vertebrates. Neurosci Comment 1:39–55Google Scholar
  33. Haydon PG, McCobb DP, Kater SB (1984): Serotonin selectively inhibits growth cone motility and synaptogenesis of specific identified neurons. Science 226:561–564Google Scholar
  34. Haydon PG, McCobb DP, Kater SB (1987): Regulation of neurite outgrowth, growth cone motility, and electrical synaptogenesis by serotonin. J Neurobiol 18:197–215Google Scholar
  35. Heimer L, Zaborszky L (1989): Neuroanatomical Tract-Tracing Methods 2: Recent Progress. New York: PlenumGoogle Scholar
  36. Hendry SHC, Jones EG, DeFelipe J, Schmechel D, Brandon C, Emson PC (1984): Neuropeptide-containing neurons of the cerebral cortex are also GABAergic. Proc Natl Acad Sci USA 81:6526–6530Google Scholar
  37. Heumann D, Leuba G, Rabinowicz T (1978): Postnatal development of the mouse cerebral neocortex. IV. Evolution of the total cortical volume, of the population of neurons and glial cells. J Hirnforsch 19:385–393Google Scholar
  38. Hohmann CF, Kwiterovich KK, Oster-Granite ML, Coyle JT (1991): Newborn basal forebrain lesions disrupt cortical cytodifferentiation as visualized by rapid Golgi staining. Cereb Cortex 1:143–157Google Scholar
  39. Horton HL, Levitt P (1988): A unique protein is expressed on early developmental limbic system axons and cortical targets. J Neurosci 8:4653–4661Google Scholar
  40. Jacobson M (1991): Developmental Neurobiology. New York: PlenumGoogle Scholar
  41. Johnson EM Jr, Chang JY, Kioke T, Martin DP (1989): Why do neurons die when deprived of trophic factors? Neurobiol Aging 10:549–552Google Scholar
  42. Keller F, Rimvall K, Barbe MF, Levitt P (1989): A membrane glycoprotein associated with the limbic system mediates the formation of the septo-hippocampal pathway in vitro. Neuron 3:551–561Google Scholar
  43. LaMour Y, Dutar P, Jobert A (1982): Topographic organization of basal forebrain neurons projecting to the rat cerebral cortex. Neurosci Lett 34:117–122Google Scholar
  44. Lauder JM, Bloom FE (1974): Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat. J Comp Neurol 155:469–482Google Scholar
  45. Leuba G, Heumann D, Rabinowicz T (1977): Postnatal development of the mouse cerebral neocortex. I. Quantitative cytoarchitectonics of some motor and sensory areas. J Hirnforsch 18:461–481Google Scholar
  46. Levey AI, Wainer BH, Mufson EJ, Mesulam MM (1983): Co-localization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum. Neuroscience 9:9–22Google Scholar
  47. Levitt P (1984): A monoclonal antibody to limbic system neurons. Science 223:229–301Google Scholar
  48. Levitt P, Moore RY (1979): Development of the noradrenergic innervation of neocortex. Brain Res 162:243–259Google Scholar
  49. Lidov HGW, Grzanna R, Molliver ME (1980): The serotonin innervation of the cerebral cortex in the rat—an immunohistochemical analysis. Neuroscience 5:207–227Google Scholar
  50. Lidov HGW, Molliver ME (1982): The structure of cerebral cortex in the rat following prenatal administration of 6-hydroxydopamine. Dev Brain Res 3:81–108Google Scholar
  51. Lidov HGW, Molliver ME, Zecevic NR (1978): Characterization of the monoaminergic innervation of immature rat neocortex: A histo-fluorescence analysis. J Comp Neurol 181:663–680Google Scholar
  52. Luiten PGM, Gaykema RPA, Traber J, Spencer DG Jr (1987): Cortical projection patterns of magnocellular basal nucleus subdivisions as revealed by anterogradely transported Pha-seolus vulgaris leucoagglutinin. Brain Res 413:229–250Google Scholar
  53. Luskin MB, Pearlman AL, Sanes JR (1988): Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1:635–647Google Scholar
  54. Maeda T, Tohyama M, Shimizu N (1974): Modification of postnatal development of neocortex in rat brain with experimental deprivation of locus coeruleus. Brain Res 70:515–520Google Scholar
  55. Marin-Padilla M (1978): Dual origin of the mammalian neocortex and evolution of the cortical-plate. Anat Embryol 152:109–126Google Scholar
  56. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG, Johnson EM Jr (1988): Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 106:829–844Google Scholar
  57. Martin DP, Wallace TL, Johnson EM Jr (1989): Neuronal death caused by nerve growth factor deprivation results from a cascade of new RNA and protein synthesis. J Neurosci 10:184–192Google Scholar
  58. McCobb DP, Haydon PG, Kater SB (1988): Dopamine and serotonin inhibition of neurite elongation of different identified neurons. J Neurosci Res 19:19–26Google Scholar
  59. Meineke D, Schwartz ML, Rakic P (1991): GA-BAergic cortical neurons express their transmitter phenotype during migration and early cortical plate formation in developing monkey. Soc Neurosci Abstr 17:1479Google Scholar
  60. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983): Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Chl-Ch6). Neuroscience 10:1185–1201Google Scholar
  61. Miller MW (1981): Maturation of the rat visual cortex. I. A quantitative study of Golgi-impregnated pyramidal neurons. J Neurocytol 10:859–878Google Scholar
  62. Miller MW (1985): Co-generation of projection and local circuit neurons in neocortex. Dev Brain Res 23:187–192Google Scholar
  63. Miller MW (1986a): Fetal alcohol effects on the generation and migration of cerebral cortical neurons. Science 233:1308–1311Google Scholar
  64. Miller MW (1986b): Maturation of the rat visual cortex. III. Postnatal morphogenesis and syn-aptogenesis of local circuit neurons. Dev Brain Res 25:271–285Google Scholar
  65. Miller MW (1988a): Development of projection and local circuit neurons in neocortex. In: Cerebral Cortex, Peters A, Jones EG, eds. New York: Plenum, Vol 7, pp 133–175Google Scholar
  66. Miller MW (1988b): Effect of prenatal exposure to ethanol on the development of cerebral cortex: I. Neuronal generation. Alcoholism: Clin Exp Res 12:440–449Google Scholar
  67. Miller MW (1988c): Maturation of rat visual cortex. IV. Generation, migration, morphogenesis and connectivity of a typically oriented pyramidal neurons. J Comp Neurol 274: 387–405Google Scholar
  68. Miller MW (1992): Migration of peptide-immunoreactive local circuit neurons to rat cingulate cortex. Cereb Cortex 2:444–455Google Scholar
  69. Miller MW, Al-Ghoul WM, Murtaugh M (1991): Expression of ALZ-50-immunoreactivity in the developing principal sensory nucleus of the trigeminal nerve: Effect of transecting the infraorbital nerve. Dev Brain Res 560:132–138Google Scholar
  70. Moore RY, Loy R (1978): Fluorescence histochemistry. In: Neuroanatomical Research Techniques, Robertson RT, ed. New York: Academic Press, pp 115–139Google Scholar
  71. Morrison JH, Grzanna R, Molliver ME, Coyle JT (1978): The distribution and orientation of noradrenergic fibers in neocortex of the rat: An immunofluorescence study. J Comp Neurol 181:17–40Google Scholar
  72. Naegele JR, Barnstable CJ, Wahle PA (1991): Expression of a unique 56-kDa polypeptide by neurons in the subplate zone of the developing cerebral cortex. Proc Natl Acad Sci USA 88:330–334Google Scholar
  73. Oh LJ, Kim G, Yu J, Robertson RT (1991): Transneuronal degeneration of thalamic neurons following deafferentation: Quantitative studies using [3H]thymidine autoradiography. Dev Brain Res 63:191–200Google Scholar
  74. Parnavelas JG, Papadopoulos GC, Cavanaugh ME (1988): Changes in neurotransmitters during development. In: Cerebral Cortex, Peters A, Jones EG, eds. New York: Plenum, Vol 7, pp 177–209Google Scholar
  75. Petracca FM, Baskin DG, Diaz J, Dorsa DM (1986): Ontogenic changes in vasopressin binding site distribution in rat brain: An autoradiographic study. Dev Brain Res 28:63–68Google Scholar
  76. Price JL, Stern R (1983): Individual cells in the nucleus basalis-diagonal band complex have restricted axonal projections to the cerebral-cortex in the rat. Brain Res 269:352–356Google Scholar
  77. Purves D, Lichtman JW (1985): Principles of Neural Development Sunderland, MA: SinauerGoogle Scholar
  78. Reisert I, Schuster RJ, Zienecker RJ, Pilgrim C (1990): Prenatal development of mesencephalic and diencephalic dopaminergic systems in the male and female rat. Dev Brain Res 53:222–229Google Scholar
  79. Rhoades RW, Bennett-Clarke CA, Chiaia NL, White FA, Macdonald GJ, Haring JH, Jacquin MF (1990): Development and lesion induced reorganization of the cortical representation of the rat’s body surface as revealed by immu-nocytochemistry for serotonin. J Comp Neurol 293:190–207Google Scholar
  80. Ribak CE (1978): Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase. J Neurocytol 7:461–478Google Scholar
  81. Richter W (1980): Neurohistologische und mor-phometrische Untersuchungen der Ontogenese der Regio cingularis mesoneocorticalis der Ratte. J Hirnforsch 21:53–87Google Scholar
  82. Rickmann M, Chronwall BM, Wolff JR (1977): On the development of non-pyramidal neurons and axons outside the cortical plate: The early marginal zone as a palliai anlage. Anat Embryol 151:285–307Google Scholar
  83. Robertson RT (1978): Neuroanatomical Research Techniques. New York: Academic PressGoogle Scholar
  84. Robertson RT (1987): A morphogenic role for transiently expressed acetylcholinesterase in thalamocortical development? Neurosci Lett 75:259–264Google Scholar
  85. Robertson RT, Hanes MA, Yu J (1988): Investigations of the origins of acetylcholinesterase activity in developing rat visual cortex. Dev Brain Res 41:1–23Google Scholar
  86. Robertson RT, Kageyama GH, Gallardo KA, Yu J (1990): Development of basal forebrain cholinergic projections to cerebral cortex; AChE histochemical studies in rats and hamsters. Soc Neurosci A bstr 16:1151Google Scholar
  87. Robertson RT, Tijerina AA, Callaway JL (1983): Development of acetylcholinesterase activity in ventral retrosplenial cortex of the rat. Anat Rec 205:164AGoogle Scholar
  88. Saper CB (1984): Organization of cerebral cortical afferent systems in the rat. I. Magnocel-lular basal nucleus. J Comp Neurol 222:313–342Google Scholar
  89. Schambra UB, Sulik KK, Petrusz P, Lauder JM (1989): Ontogeny of cholinergic neurons in the mouse forebrain. J Comp Neurol 288:101–122Google Scholar
  90. Schlumpf M, Shoemaker WJ, Bloom FE (1980): Innervation of embryonic rat cerebral cortex by catecholamine-containing fibers. J Comp Neurol 192:361–376Google Scholar
  91. Schmidt RH, Björklund A, Lindvall O, Lorén I (1982): Prefrontal cortex: Dense dopaminergic input in the newborn rat. Dev Brain Res 5:222–228Google Scholar
  92. Semba K, Fibiger HC (1988): Time of origin of cholinergic neurons in the rat basal forebrain. J Comp Neurol 269:87–95Google Scholar
  93. Senft SL, Woolsey T (1991): Computer-aided analyses of thalamocortical afferent ingrowth. Cereb Cortex 1:140–166Google Scholar
  94. Smart IHM (1983): Three dimensional growth of mouse isocortex. J Anat 137:683–694Google Scholar
  95. Sperry RW (1963): Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 50:703–710Google Scholar
  96. Tengelsen LA, Robertson RT (1982): Distribution and thalamic origin of acetylcholinesterase activity in retrosplenial cortex of the rat. Soc Neurosci Abstr 8:211Google Scholar
  97. Thompson SM, Robertson RT (1987): Organization of subcortical pathways for sensory projections to limbic cortex. I. Subcortical projections to limbic cortex in the rat. J Comp Neurol 265:175–188Google Scholar
  98. Tribollet E, Charpak S, Schmidt A, Dubois-Dauphin M, Dreifuss JJ (1989): Appearance and transient expression of oxytocin receptors in fetal, infant, and peripubertal rat brain studied by autoradiography and electrophysiol-ogy. J Neurosci 9:1764–1773Google Scholar
  99. Trumpy JH (1971): Transneuronal degeneration in the pontine nuclei of the cat. I. Neuronal changes in animals of varying ages. Ergeb Anat Entwicklungsgesch 44:1–46Google Scholar
  100. Ueda K, Masliah E, Saitoh T, Bakalis SL, Scobie H, Kosik KS (1990): Alz-50 recognizes a phos-phorylated epitope of tau protein. J Neurosci 10:3295–3304Google Scholar
  101. Valverde FL, Lopez-Mascaraque L, De Carlos JA (1990): Distribution and morphology of Alz-50-immunoreactive cells in the developing visual cortex of kittens. J Neurocytol 19:662–671Google Scholar
  102. van Eden CG (1985): Postnatal development of rat prefrontal cortex. Doctoral dissertation, Rodopi, Amsterdam.Google Scholar
  103. van Eden CG, Uylings HBM, Van Pelt J (1984): Sex-difference and left-right asymmetries in the prefrontal cortex during postnatal development in the rat. Dev Brain Res 12:146–153Google Scholar
  104. Verney C, Berger B, Adrien J, Vigny A, Gay M (1982): Development of the dopaminergic innervation of the rat cerebral cortex: A light microscopic immunocytochemical study using anti-tyrosine hydroxylase antibodies. Dev Brain Res 5:41–52Google Scholar
  105. Verney C, Berger B, Baulac M, Helle KM, Alvarez C (1984): Dopamine-ß-hydroxylase-like immunoreactivity in the fetal cerebral cortex of the rat: Noradrenergic ascending pathways and terminal fields. Int J Dev Neurosci 2:491–503Google Scholar
  106. Vogt BA, Miller MW (1983): Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216:182–210Google Scholar
  107. Vogt BA, Peters A (1981): Form and distribution of neurons in rat cingulate cortex: areas 32, 24 and 29. J Comp Neurol 195:603–625Google Scholar
  108. Walsh C, Cepko CL (1988): Clonally related cortical cells show several migration patterns. Science 241:1342–1345Google Scholar
  109. Wenk H (1989): Ontogentische Untersuchungen der cholinergin Innervation der Grosshirnrinde bei Ratten. J Hirnforsch 30:281–289Google Scholar
  110. White E, Rock MP (1980): Three-dimensional aspects and synaptic relationships of a Golgi-impregnated spiny stellate cell reconstructed from serial thin sections. J Neurocytol 9:1217–1230Google Scholar
  111. Williams RW, Herrup K (1988): The control of neuron number. Annu Rev Neurosci 11:423–453Google Scholar
  112. Wolozin BL, Pruchnicki A, Dickson DW, Davies P (1986): A neuronal antigen in the brain of Alzheimer’s patients. Science 232:648–650Google Scholar
  113. Wolozin BL, Scicutella A, Davies P (1988): Re-expression of a developmentally regulated protein in Alzheimer’s disease and Down’s syndrome. Proc Natl Acad Sci USA 85:6202–6206Google Scholar
  114. Woolf NJ (1991): Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475–524Google Scholar
  115. Zacco A, Cooper V, Chantier PD, Fisher-Hyland S, Horton HL, Levitt P (1990): Isolation, biochemical characterization and ultrastructural analysis of the limbic system-associated membrane protein, a protein expressed by neurons comprising functional neural circuits. J Neurosci 10:73–90Google Scholar
  116. Zecevic NR, Molliver ME (1978): The origin of the monoaminergic innervation of immature rat neocortex: An ultrastructural analysis following lesions. Brain Res 150:387–397Google Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Michael W. Miller
  • Richard T. Robertson

There are no affiliations available

Personalised recommendations