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Ontogenesis of the laminar structure in areas 17 and 18 of the human visual cortex

A quantitative study

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Summary

A quantitative morphological study of the pre-and postnatal development in the primary (area 17) and secondary (area 18) visual cortical regions was performed on 108 human brains. The neuropil proportion and thickness were measured with an image analyzer for the different cortical layers and the resulting data were approximated with logistic growth functions. The different layers show a marked heterochrony both within and between the areas. The neuropil proportion of layer 1 is the compartment to develop first in both areas. It has the lowest growth velocity, followed by layer VI and layers V, IV, III and II. This maturational sequence reflects the sequence of appearance of immature neurons during the migration period of neocortical ontogenesis. The development of the neuropil proportion is highly synchronized between areas 17 and 18 during the prenatal period, but in the first postnatal weeks, area 17 grows more quickly than area 18. Later on, this relation is reversed and area 18 reaches adult values of neuropil proportions about three months earlier than area 17. The growth in thickness of all layers is complated later than the growth in neuropil proportion. The growth in layer thickness is completed in Area 18 about two months earlier than in area 17, although area 18 has a greater cortical thickness. The results are compared with data on growth in volume, dendritic arborization and the development of visual function.

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References

  • Becker LE, Armstrong DL, Chan F, Wood MM (1984) Dendritic development in human occipital cortical neurons. Dev Brain Res 13:117–124

    Google Scholar 

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

    Google Scholar 

  • Bethmann IR (1978) Die Area parastriata des Menschen. Medizin Diss Kiel

  • Bischoff TLW (1880) Hirngewicht des Menschen. Anatomische physiologische und physikalische Tabellen. Neusser, Bonn

    Google Scholar 

  • Bok ST (1929) Der Einfluß der in den Furchen und Windungen auftretenden Krümmungen der Großhirnrinde auf die Rindenarchitektur. Z Ges Neurol Psychiat 121:682–750

    Google Scholar 

  • Boothe RG, Dobson V, Teller DY (1985) Postnatal development of vision in human and nonhuman primates. Annu Rev Neurosci 8:495–545

    Google Scholar 

  • Braak E (1982) On the structure of the human striate area. Adv Anat Embryol Cell Biol 77:1–86

    Google Scholar 

  • Braak H (1976) On the striate area of the human isocortex. A Golgi- and pigmentarchitectonic study. J Comp Neurol 166:341–364

    Google Scholar 

  • Braak H (1984) Architectonics as seen by lipofuscin stains. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Plenum Press, New York London, pp 59–104

    Google Scholar 

  • Brodmann K (1909) Vergleichende Lokalisationslehre der Grßhirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Barth JA, Leipzig

    Google Scholar 

  • Büsching U (1983) Zur Ontogenese der Area striata des Menschen. Medizin Diss Kiel

  • Conel JL (1939–1968) The postnatal development of the human cerebral cortex, vol I–VIII. Harvard University Press, Cambridge

    Google Scholar 

  • De Courten C, Leuba G, Huttenlocher PR, Garey L, Van der Loos H (1982) Volumetric, neuronal and synaptic development of human primary visual cortex. Neurosci Lett [Suppl] 10:135

    Google Scholar 

  • Eins S, Wilhelms E (1976) Assessment of preparative volume changes in central nervous tissue using automatic image analysis. Microscope 24:29–38

    Google Scholar 

  • Filmonoff JN (1929) Zur embryonalen und postembryonalen Entwicklung der Großhirnrinde des Menschen. J Psychol Neurol 39:323–389

    Google Scholar 

  • Filimonoff JN (1932) Über die Variabilität der Großhirnrindenstruktur. Mitteilung II. J Psychol Neurol 44:1–96

    Google Scholar 

  • Fischer G, Köhler Chr, Röthig W, Rojewski H (1973) Die Gewichtsveränderung von Gehirnen während einer 4-wöchigen Formalinfixierung in Abhängigkeit von Alter, Geschlecht und Liegezeit post mortem. Zentralbl Allg Pathol 117:400–407

    Google Scholar 

  • Flechsig P (1927) Meine myelogenetische Hirnlehre mit biographischer Einleitung. Springer, Berlin

    Google Scholar 

  • Foh E, Haug H, König M, Rast A (1973) Quantitative Bestimmung zum feineren Aufbau der Sehrinde der Katze. Zugleich ein methodischer Beitrag zur Messung des Neuropils. Microsc Acta 72:148–168

    Google Scholar 

  • Garey LJ (1983) Development of visual system — comparison of monkey and man. Acta Morphol Hungarica 31:27–38

    Google Scholar 

  • Garey LJ (1984) Structural development of the visual system of man. Human Neurobiol 3:75–80

    Google Scholar 

  • Garey LJ, De Courten C (1983) Structural development of the lateral geniculate nucleus and visual cortex in monkey and man. Behav Brain Res 10:3–13

    Google Scholar 

  • Gladstone RJ (1905) A study of the relation of the brain to the size of the head. Biometrika 4:105–123

    Google Scholar 

  • Haug H (1958) Quantitative Untersuchungen an der Sehrinde. Thieme, Stuttgart

    Google Scholar 

  • Haug H (1979) The evaluation of cell-densities and of nerve-cell size distribution by stereological procedures in a layered tissue (cortex cerebri). Microsc Acta 82:147–161

    Google Scholar 

  • Haug H (1980) Die Abhängigkeit der Einbettungsschrumpfung des Gehirngewebes vom Lebensalter. Verh Anat Ges 74:699–700

    Google Scholar 

  • Haug H (1984) Macroscopic and microscopic morphometry of the human brain and cortex. A survey in the light of new results. In: Pilleri G, Tagliavini F (eds) Brain pathology, vol 1, pp 123–149

  • Haug H, Kühl S, Mecke E, Sass NL, Wasner K (1984) The significance of morphometric procedures in the investigation of age changes in cytoarchitectonic structures of the human brain. J Hirnforsch 25:353–374

    Google Scholar 

  • Jacobson M (1978) Developmental neurobiology. Plenum Press, New York London

    Google Scholar 

  • Kahle W (1969) Die Entwicklung der menschlichen Großhirnhemisphäre. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Kostovic I, Rakic P (1984) Development of peristriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesteras staining. J Neurosci 4:25–42

    Google Scholar 

  • Kraus C (1962) Veränderungen der Paraffinschnitte durch das Mikrotomieren und das nachfolgende Aufziehen. J Hirnforsch 5:23–28

    Google Scholar 

  • Kretschmann HJ, Wingert F (1971) Computeranwendungen bei Wachstumsproblemen in Biologie und Medizin. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Kretschmann HJ, Schleicher A, Grottschreiber JF, Kullmann W (1979) The Yakovlev collection — a pilot study of its suitability for the morphometric documentation of the human brain. J Neurol Sci 43:111–126

    Google Scholar 

  • Kretschmann HJ, Kammradt G, Cowart EC, Hopf A, Krauthausen I, Lange HW, Sauer B (1982) The Yakovlev collection. A unique resource for brain research and the basis for a multinational data bank. J Hirnforsh 23:647–656

    Google Scholar 

  • Larroche JC (1981) The marginal layer in the neocortex of a 7 week-old human embryo. A light and electron microscopic study. Anat Embryol 162:301–312

    Google Scholar 

  • Leibnitz L (1972) Untersuchungen zur Optimierung der Gewichts-und Volumenänderungen von Hirnen während der Fixierung, Dehydrierung und Aufhellung sowie über Rückschlüsse vom Gewicht des behandelten auf das Volumen des frischen Gehirns. J Hirnforsch 13:320–329

    Google Scholar 

  • Magoon EH, Robb RM (1981) Development of myelin in human optic nerve and tract: a light and electron microscopic study. Arch Ophthalmol 99:655–659

    Google Scholar 

  • Marin-Padilla M (1971) 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

    Google Scholar 

  • Marin-Padilla M (1978) Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat Embryol 152:109–126

    Google Scholar 

  • Marin-Padilla M (1983) Structural organization of the human cerebral cortex prior to the appearance fo the cortical plate. Anat Embryol 168:21–40

    Google Scholar 

  • Marin-Padilla M, Marin-Padilla TM (1982) Origin, prenatal development and structural organization of layer I of the human cerebral (motor) cortex. A Golgi study. Anat Embryol 164:161–206

    Google Scholar 

  • Matiegka H (1902) Über das Hirngewicht, die Schädelkapazität, sowie deren Beziehungen zur psychischen Tätigkeit des Menschen. Sitzungsber Böhm Wiss Math Naturwiss K1 20:1–75

    Google Scholar 

  • Michel AE, Garey LJ (1984) The development of dendritic spines in the human visual cortex. Hum Neurobiol 3:223–227

    Google Scholar 

  • Molliver ME, Kostovic I, van der Loos H (1973) The development of synapses in cerebral of the human fetus. Brain Res 50:403–497

    Google Scholar 

  • Mouritzen Dam AM (1979) Shrinkage of the brain during histological procedures with fixation in formaldehyde solutions of different concentrations. J Hirnforsch 20:115–119

    Google Scholar 

  • Paul F (1971) Biometrische Analyse der Volumina des Prosencephalon und der Großhirnrinde von 31 menschlichen, adulten Gehirnen. Z Anat Entwickl Gesch 133:325–360

    Google Scholar 

  • Poliakov GI (1961) Some results of research into the development of the neuronal structure of the cortical ends of the analyzers in man. J Comp Neurol 117:197–212

    Google Scholar 

  • Powell TPS (1981) Certain aspects of the intrinsic organization of the cerebral cortex. In: Pompeiano O, Marsan CA (eds) Brain mechanisms and perceptual awareness. Raven Press, New York, pp 1–19

    Google Scholar 

  • Pratt WK (1978) Digital image processing. Wiley, New York

    Google Scholar 

  • Purpura DP (1975) Morphogenesis of visual cortex in preterm infant. In: Brazier MA (ed) Growth and development of the brain. Raven Press, New York, pp 33–49

    Google Scholar 

  • Rabinowicz T (1967) The cerebral cortex of premature infat of the 8th month. Prog Brain Res 4:39–86

    Google Scholar 

  • Sass NL (1982) The age-dependent variation of the embedding-shrinkage of neurohistological sections. Mikroskopie 39:278–281

    Google Scholar 

  • Sauer B (1983a) Semi-automatic analysis of microscopic images of the human cerebral cortex using the grey level index. J Microsc 129:75–87

    Google Scholar 

  • Sauer B (1983b) Lamina boundaries of the human striate area compared with automatically — obtained grey level index profiles. J Hirnforsch 24:79–87

    Google Scholar 

  • Sauer B (1983c) Quantitative analysis of the laminae of the striate area in man. An application of automatic image analysis. J Hirnforsch 24:89–97

    Google Scholar 

  • Sauer B, Kammradt G, Krauthausen I, Kretschmann HJ, Lange HW, Wingert F (1983) Qualitative and quantitative development of the visual cortex in man. J Comp Neurol 214:441–450

    Google Scholar 

  • Schleicher A, Zilles K, Kretschmann HJ (1978) Automatische Registrierung und Auswertung eines Grauwertindex in histologischen Schnitten. Verh Anat Ges 72:413–415

    Google Scholar 

  • Schwientek P (1985) Quantitative Analyse des arealen und laminären Aufbaus des Isocortex der Ratte. Medizin Diss Köln

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

    Google Scholar 

  • Skullerud K (1985) Variations in the size of the human brain. Acta Neurol Scand [Suppl 102] 71:1–94

    Google Scholar 

  • Swadlow HA (1983) Efferent systems of primary visual cortex: a review of structure and function. Brain Res Rev 6:1–24

    Google Scholar 

  • v. Economo C, Koskinas GN (1925) Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Springer, Wien

    Google Scholar 

  • Wessely W (1970) Biometrische Analyse der Frischvolumina des Rhombencephalon, des Cerebellum und der Ventrikel von 31 menschlichen, adulten Gehirnen. J Hirnforsch 12:11–28

    Google Scholar 

  • Wree A, Zilles K, Schleicher A (1980) Analyse der laminären Struktur der Area striata mit verschiedenen stereologischen Meßmethoden. Verh Anat Ges 74:727–728

    Google Scholar 

  • Wree A, Schleicher A, Zilles (1982) Estimation of volume fractions in nervous tissue with an image analyzer. J Neurosci Meth 6:29–43

    Google Scholar 

  • Yakovlev PI, Lecours AG (1967) The myelogenetic cycles of the regional maturation of the brain. In: Minkowsky A (ed) Regional development of the brain in early life. Blackwell, Oxford

    Google Scholar 

  • Zilles K (1972) Biometrische Analyse der Frischvolumina verschiedener prosencephaler Hirnregionen von 78 menschlichen, adulten Gehirnen. Gegenbaurs Morphol Jahrb 118:234–273

    Google Scholar 

  • Zilles K, Schleicher A (1980) Quantitative Analyse der laminären Struktur menschlicher Cortexareale. Verh Anat Ges 74:725–726

    Google Scholar 

  • Zilles K, Schleicher A, Kretschmann HJ (1978a) A quantitative approach to cytoarchitectonics. I. The areal pattern ofthe cortex of Tupaia belangeri. Anat Embryol 153:195–212

    Google Scholar 

  • Zilles K, Schleicher A, Kretschmann HJ (1978b) A quantitative approach to cytoarchitectonics. II. The allocortex of Tupaia belangeri. Anat Embryol 154:335–352

    Google Scholar 

  • Zilles K, Schleicher A, Kretschmann HJ (1978c) Quantitative Darstellung cytoarchitektonischer Areale im Cortex von Tupaia belangeri und SPF-Katze. Verh Anat Ges 72:409–411

    Google Scholar 

  • Zilles K, Schleicher A, Büsching U, Benoit W (1981) Ontogenese der laminären Struktur in der Area striata des Menschen. Verh Anat Ges 75:935–936

    Google Scholar 

  • Zilles K, Stephan H, Schleicher A (1982) Quantitative cytoarchitectonics of the cerebral cortices of several prosimian species. In: Armstrong E, Falk D (eds) Primate brain evolution. Methods and concepts. Plenum Press, New York London, pp 177–201

    Google Scholar 

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Supported by the Deutsche Forschungsgemeinschaft, grant Zi 192/4-4, 5-4 and by the Ministerium für Wissenschaft und Forschung des Landes Nordrhein-Westfalen

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Zilles, K., Werners, R., Büsching, U. et al. Ontogenesis of the laminar structure in areas 17 and 18 of the human visual cortex. Anat Embryol 174, 339–353 (1986). https://doi.org/10.1007/BF00698784

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