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Anatomy and Embryology

, Volume 152, Issue 2, pp 109–126 | Cite as

Dual origin of the mammalian neocortex and evolution of the cortical plate

  • Miguel Marin-Padilla
Article

Summary

A Golgi study of the structural organization of the early developmental stages of the cerebral cortex of the cat has been presented. It has been demonstrated that the structural organization of the mammalian neocortex undergoes a series of fundamental transformations in the course of its early embryonic development. A clear understanding of these early structural changes is essential to comprehend the multi-layered nature of the mammalian cerebral cortex. In order of appearance the following basic transformations have been recognized in mammalian cortical ontogenesis. A. The first recognizable change in the undifferentiated neuroepithelial structure of the cerebral vesicle is the arrival and penetration of corticipetal fibers through its superficial region. The penetration of these afferent fibers into the cerebral vesicle forms a clear plexiform region under the pial surface just above the matrix zone. This clear plexiform region corresponds to the classical marginal zone and is composed, at first, of corticipetal fibers and their collaterals. B. The arrival of these corticipetal fibers induces maturation of some neurons. Primitive-looking and still-developing neurons begin to appear scattered among the afferent fibers without forming any distinct lamination. This combination of an external white matter of afferent fibers with scattered neurons among the fibers has been named the primordial plexiform layer of the mammalian cerebral cortex. Its structure represents a primitive type of nervous organization which is reminiscent of the amphibian brain. In mammalian cortical ontogenesis this primitive plexiform layer has a short duration and it is established as a distinct structure prior to the appearance of the cortical plate. C. The appearance and the formation of the cortical plate within the primordial plexiform layer results in the separation of its neurons and fibers into a superficial and a deep plexiform lamination. Structural and functional interrelationships soon start to develop between the neuronal elements of the superficial and the deep plexiform laminations establishing the primordial neocortical organization, which is characterized by specific types of neurons and fibers. Its structural organization resembles somewhat that of the cerebral cortex of some reptiles. It is important to emphasize that the neurons and fibers of this primordial neocortical organization persist and become components of the adult cerebral cortex. The superficial plexiform becomes layer I and the deep lamination becomes layer VII of the adult mammalian cerebral cortex. Therefore, the cortical plate represents the primordium of only layers VI, V, IV, III, and II of the adult cerebral cortex. The cortical plate is considered to be a distinct mammalian structure of a more recent phylogenetic origin. D. The last significant transformation consists of the sequential growth and maturation of the cortical plate which follows an “inside-out” progression. The maturation of the neurons of the cortical plate and hence the formation of its laminations seems to be due to the sequential and progressive arrival of corticipetal fibers which takes place during the late embryonic stages of development.

According to these observations the mammalian cerebral cortex has a double origin and a possible dual nature. A new interpretation of the basic structural organization of the mammalian neocortex based primarily on this dual nature is introduced and analyzed in this communication. It proposes new ideas concerning the origin, the embryonic development, and the phylogenetic evolution of the mammalian cerebral cortex which differ somewhat from the classical conceptions of cortical development.

Key words

Origin Development Cerebral cortex Mammals 

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References

  1. Åström, K.E.: On the early development of the isocortex in fetal sheep. In: Developmental Neurology (C.C. Bernhard and J.P. Schade, eds.). Progress in Brain Res. 26, 1–59 (1967)Google Scholar
  2. Angevine, J.B. Jr.: Time of origin of neurons of the hippocampal region. An autoradiographic study in the mouse. Exp. Neurol. Suppl. 2, 1–70 (1965)Google Scholar
  3. Angevine, J.B. Jr., Sidman, R.L.: Autoradiographic study of cell migration during histogenesis of cerebral cortex of the mouse. Nature (London). 192, 766–768 (1961)Google Scholar
  4. Bailey, P., Von Bonin, G.: The Isocortex of Man, pp. 61–80. Chicago: University of Illinois Press 1951Google Scholar
  5. Berry, M., Rogers, A.W.: The migration of neuroblasts in the developing cerebral cortex. J. Anat. 99, 691–709 (1965)Google Scholar
  6. Blinkov, S.M., Glezer, I.I.: The Human Brain in Figures and Tables (English translation, Basil Haigh), pp. 394–388. New York: Basic Book Inc. Publs. Plenum Press, 1968Google Scholar
  7. Boulder Committee: Embryonic vertebrate central nervous system: Revised terminology. Anat. Rec. 166, 257–261 (1970)Google Scholar
  8. Brückner, G., Mareŝ, B., Biesold, D.: Neurogenesis in the central visual system of the rat. An autoradiographic investigation. J. Comp. Neurol. 166, 245–256 (1976)Google Scholar
  9. Cajal, S.R.: Histologie du systéme nerveux de l'homme et des vertébrès (reprinted Madrid. 1952) vol. II, pp. 519–598. Paris: Maloine 1911Google Scholar
  10. Colby, D.E.: Induced estrus and time pregnancy in cats. Lab. Amin. Care. 20, 1075–1080 (1970)Google Scholar
  11. Godina, G.: Istogenesi e differenziazione dei neuroni e degli elementi gliale della corteccia cerebrale. Z. Zellforsch. 36, 401–435 (1951)Google Scholar
  12. His, W.: Die Entwicklung des Menschlichen Gehirns während der estern Monate, pp. 176–179. Leipzig: Hirzel. 1904Google Scholar
  13. Jones, E.G.: Lamination and differentiatial distribution of thalamic afferents within the sensory-motor cortex of the squire monkey. J. Comp. Neurol. 160, 167–204 (1975)Google Scholar
  14. Koelliker, A.: Handbuch der Gewebelehre des Menschen. Nervousystem des Menschen und der Thiere, pp. 409. Leipzig: Engelman 1896Google Scholar
  15. König, N., Roch, G., Marty, R.: The onset of synaptogenesis in the rat temporal cortex. Anat. Embryol. 148, 73–87 (1975)Google Scholar
  16. König, N., Valat, J., Fulcrand, J., Marty, R.: The time of origin of Cajal-Retzius cells in the rat temporal cortex. An autoradiographic study. Neuroscience Letters 4, 21–26 (1977)Google Scholar
  17. Lorente de Nó, R.: Corteza cerebral del raton. I. La corteza acustica. Trab. Lab. Invest. Biol. 20, 41–78 (1922)Google Scholar
  18. Lorente de Nó, R.: Cerebral cortex: Architecture, intracortical connections, motor projection. In: Physiology of the Neurvous System (J.F. Fulton, ed.), pp. 274–313. New York: Oxford Univ. Press 1943Google Scholar
  19. Marin-Padilla, M.: Prenatal and early postnatal ontogenesis of the human motor cortex. A Golgi study. I. The sequential development of the cortical layers. Brain Res. 23, 167–183 (1970)Google Scholar
  20. Marin-Padilla, M.: Prenatal and early postnatal ontogenesis of the human motor cortex. II. The basketpyramidal system. Brain Res. 23, 185–191 (1970)Google Scholar
  21. Marin-Padilla, M.: Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study. I. The primordial neocortical organization. Z. Anat. Entwickl.-Gesch. 134, 117–145 (1971)Google Scholar
  22. Marin-Padilla, M.: Prenatal ontogenetic history of the principal neurons of the neocortex of the cat (Felis domestica). A Golgi study. II. Developmental differences and their significance. Z. Anat. Entwickl.-Gesch. 136, 125–142 (1972)Google Scholar
  23. Molliver, M.E., Van der Loos, H.: The ontogenesis of cortical circuitry: The spatial distribution of synapses in somesthetic cortex of the newborn dog. In: Advances in anatomy, embryology and cell biology. Vol. 42, pp. 7–54. Berlin, Heidelberg, New York: Springer-Verlag 1970Google Scholar
  24. Molliver, M.E., Kostovic, I., Van der Loos, H.: The development of synapses in the cerebral cortex of the human fetus. Brain Res. 50, 403–407 (1973)Google Scholar
  25. Persson, H.E.: Development of somatosensory cortical function. An electrophysiological study in prenatal sheep. Acta Physiolo. Scand. Suppl. 394, 1–64 (1973)Google Scholar
  26. Poliakov, G.I.: Some results of research into the development of the neuronal structure of the cortical ends of the analysers in man. J. Comp. Neurol. 117, 197–212 (1961)Google Scholar
  27. Poliakov, G.I.: Development and complications of the cortical part of coupling mechanism in the evolution of vertebrates. J. Fur Hirnforsh. 7, 253–273 (1964)Google Scholar
  28. Poliakov, G.I.: Modern data on the structural organization of the cerebral cortex. In: Higher cortical functions in man, pp. 39–69. (English translation by Basil Haigh) New York: Basic Book, Inc. Publis. 1966Google Scholar
  29. Povlishock, J.T.: The fine structure of the axons and growth cones of the human fetal cerebral cortex. Brain Res. 114, 379–389 (1976)Google Scholar
  30. Raedler, A., Sievers, J.: Light and electron microscopic studies on specific cells of the marginal zone in developing cerebral cortex. Anat. Embryol. 149, 173–181 (1976)Google Scholar
  31. Rakic, P.: Neurons in rhesus monkey visual cortex: Systematic relation between time of origin and eventual disposition. Science. 183, 425–427 (1974)Google Scholar
  32. Rakic, P.: Timing of major ontogenetic events in the visual cortex of the rhesus monkey. In: Brain mechanisms in mental retardation (N.A. Buchwald, ed.). UCLA Forum Med. Sci. 18, 3–40 (1975)Google Scholar
  33. Ravinowicz, T.H.: The cerebral cortex of the premature infant of the 8th month. In: Growth and maturation of the brain (D.P. Purpura and J.P. Schade, eds.). Progress in Brain Res. 4, 39–92 (1964)Google Scholar
  34. Retzius, G.: Ueber den Bau der Olerflächenschicht der Grosshirnrinde beim Menschen und beiden Säugethieren. Verh. Biol. Ver. (Stolkolhom) 3, 90–103 (1891)Google Scholar
  35. Shimada, M., Langman, J.: Cell migration and differentiation in the cerebral cortex of the golden hamster. J. Comp. Neurol. 139, 227–244 (1970)Google Scholar
  36. Shkol'nik-Yarros, E.G.: Neurons and Interneuronal Connections of the central visual system, pp. 1–117 (English translation, Basil Haigh). New York: Plenum Press. 1971Google Scholar
  37. Sidman, R.L.: Cell proliferation, migration and interaction in the developing mammalian nervous system. In: The neurosciences second study program (F.O. Schmitt, ed.), pp. 100–107. New York: The Rockefeller University Press 1970Google Scholar
  38. Sidman, R.L., Rakic, P.: Neuronal migration with special reference to the developing human brain: A review. Brain Res. 62, 1–35 (1973)Google Scholar
  39. Stensaas, L.J.: The development of hippocampal and dorsolateral pallial regions of the cerebral cortex in fetal rabbits. I. Fifteen millimeters: Spongioblasts morphology. J. Comp. Neurol. 129, 59–70 (1967)Google Scholar
  40. Stensaas, L.J.: III. Twenty-nine millimeters: Marginal zone. J. Comp. Neurol. 130, 149–162 (1967)Google Scholar
  41. Stensaas, L.J.: IV. Forty-one millimeters: Intermediate lamina. J. Comp. Neurol. 131, 409–422 (1967)Google Scholar
  42. Sugita, N.: Comparative studies on the growth of the cerebral cortex. J. Comp. Neurol. 28, 511–591 (1917)Google Scholar
  43. Tilney, F.: Behavior in its relation to the development of the brain. Part II. Correlation between the development of the brain and behavior in the albino rat from embryonic states to maturity. Bull. Neurol. Inst. N.Y. 2, 252–358 (1933)Google Scholar
  44. Vignal, W.: Recherches sur le development des elements des couches corticales du cerveau et du cervelet chez l'homme et les mammiferes. Arch. Physiol. Nor. Path. (Paris). 2, 228–254 (1888)Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • Miguel Marin-Padilla
    • 1
  1. 1.Department of PathologyDartmouth Medical SchoolHanoverUSA

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