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The cellular pathology of microgyria

A Golgi analysis

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Abstract

A case of extensive classical four layered cerebral microgyria was examined in whole brain serial section using routine cell and fiber stains, and in Golgi impregnations. Golgi preparations demonstrate that microgyric cortex contains the spectrum of neurons characteristically found in normal cortex, and that they are segregated by class into horizontal laminae comparable to layers I–VI in the normal. In microgyric cortex neurons of the mid-cortical layers, variably layers III–V, are replaced by a tangential band of fibrous astrocytes. These findings confirm impressions from general cell and fiber stains that classical four layered microgyria is the result of a destructive process striking predominantly in mid-cortical regions. It must occur after migration is complete but before the development of secondary and tertiary gyri, that is, between the fifth and seventh fetal months. The cellular pathology as seen in Golgi impregnations establishes that neurons surviving above the scar are normally differentiated, aligned, and oriented. By exception, many surviving neurons at the border of the scar have attenuated dendritic arbors which are oriented tangentially. Very few axons or dendrites actually traverse the scar.

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Bibliography

  • Bankl, H., Jellinger, K.: Zentralnervöse Schäden nach fetaler Kohlenoxydvergiftung. Beitr. path. Anat.135, 350–376 (1967)

    Google Scholar 

  • Benirschke, K., Mendoza, G. R., Bazeley, P. L.: Placental and fetal manifestations of cytomegalovirus infection. Virchows Arch., Abt. B, Zellpath.16, 121–139 (1974)

    Google Scholar 

  • Bertrand, I., Gruner, J.: The status verrucosus of the cerebral cortex. J. Neuropath. exp. Neurol.14, 331–347 (1955)

    Google Scholar 

  • Bielschowsky, M.: Über Mikrogyrie. J. Psychol. Neurol. (Lpz.)22, 1–47 (1915)

    Google Scholar 

  • Bignami, A., Dahl, D.: Astrocyte specific protein and radial glia in the cerebral cortex of newborn rat. Nature (Lond.)252, 55–56 (1974)

    Google Scholar 

  • Bignami, A., Ralston, H. J.: Myelination of fibrillary astroglial processes in long term Wallerian degeneration: the possible relationship to status marmaratus. Brain Res.11, 710–713 (1968)

    Google Scholar 

  • Borit, A., Herndon, R. M.: The fine structure of plagues fibromyeliniques in ulegyria and status marmaratus. Acta neuropath. (Berl.)14, 304–311 (1970)

    Google Scholar 

  • Brann, A. W., Myers, R. E.: Central nervous system findings in the newborn monkey following severe in utero partial asphyxia. Neurology (Minneap.)25, 327–338 (1975)

    Google Scholar 

  • Brierley, J. B., Meldrum, B. S., Brown, A. W.: The threshold and neuropathology of cerebral “anoxic-ischemic” cell change. Arch. Neurol. (Chic.)29, 367–374 (1973)

    Google Scholar 

  • Cajal, S. R. y-: Sur la structury de l'écorce cérébrale de quelques mammifères. La Cellule7, 125–178 (1891).

    Google Scholar 

  • Cajal, S. R. y-: Histologie du Systéme Nerveux de l'Homme et des Vértebrés (trans. by L. Azoulay, Madrid) (reprinted 1972 by C.I.S.C.), Vol. I and II (1911)

  • Cajal, S. R. y-: Degeneration and regeneration of the nervous system. (trans. by R. M. May, New York) (reprinted 1959), Hafner, Vol. 2 (1928)

  • Catalano, L. W., Sever, J. L.: The role of viruses as causes of congenital defects. Ann. Rev. Microbiol.25, 255–282 (1971)

    Google Scholar 

  • Caviness, V. S., Jr., Evrard, P.: Occipital encephalocele: a pathologic and anatomic analysis. Acta neuropath. (Berl.)32, 245–255 (1975)

    Google Scholar 

  • Courville, C. B.: Etiology and pathogenesis of laminar cortical necrosis. Arch. Neurol. Psychiat. (Chic.)79, 7–30 (1958)

    Google Scholar 

  • Courville, C. B.: Antenatal and paranatal circulatory disorders as a cause of cerebral damage in early life. J. Neuropath. exp. Neurol.18, 115–140 (1959)

    Google Scholar 

  • Cowan, W. M.: Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous system. In: Contemporary research methods in neuroanatomy (eds. W. J. Nauta and S. O. E. Ebbesson), pp. 217–251. Berlin-Heidelberg-New York: Springer 1970

    Google Scholar 

  • Crome, L.: Microgyria. J. Path. Bact.64, 479–495 (1952)

    Google Scholar 

  • Crome, L.: Cytomegalic inclusion-body disease. Wld Neurol.2, 447–455 (1961)

    Google Scholar 

  • Crome, L., France, N. E.: Microgyria and cytomegalic inclusion disease in infancy. J. clin. Path.12, 427–434 (1959)

    Google Scholar 

  • Crome, L., Stern,J.: Pathology of mental retardation; Ed. 2, pp. 136–137. London: Churchill Livingston Ltd. 1972

    Google Scholar 

  • Dekaban, A. S.: Large defects in cerebral hemispheres associated with cortical dysgenesis. J. Neuropath. exp. Neurol.24, 512–530 (1965)

    Google Scholar 

  • DéLeon, G. A.: Observations on cerebral and cerebellar microgyria. Acta neuropath. (Berl.)20, 278–287 (1972)

    Google Scholar 

  • Derer, P., Caviness, V. S., Jr., Sidman, R. L.: Early cortical histogenesis in the primary olfactory cortex of the mouse. Anat. Rec. (Abstract) (1975)

  • Diezel, P.: Microgyrie infolge cerebraler Speicheldrüsen-Virus-Infection im Rahmen einer generalisierten Cytomegalies bei einem Säugling. Virchow Arch. path. Anat.325, 109–130 (1954)

    Google Scholar 

  • Driscoll, S. G.: Fetal infections in man. In: Comparative aspects of reproductive failure (ed. K. Benirschke), pp. 279–295. Berlin-Heidelberg-New York: Springer 1967

    Google Scholar 

  • Evrard, P., Caviness, V. S., Jr.: Extensive development defect of the cerebellum associated with posterior fossa ventriculocele. J. Neuropath. exp. Neurol.33, 385–399 (1974)

    Google Scholar 

  • Frenkel, J. K.: Pathology and pathogenesis of congenital toxoplasmosis. Bull. N. Y. Acad. Med.50, 182–191 (1974)

    Google Scholar 

  • Garey, L. J.: A light and electron-microscopic study of the visual cortex of the cat and monkey. Proc. roy. Soc. B179, 21–40 (1971)

    Google Scholar 

  • Ginsberg, M. D., Myers, R. E.: Fetal brain injury after maternal carbon monoxide intoxication. Neurology (Minneap.)26, 15–23 (1976)

    Google Scholar 

  • Greenfield, J. G., Wolfsohn, J. M.: Microcephalia vera. A study of two brains illustrating the agyric form and the complex microgyric form. Arch. Neurol. Psychiat. (Chic.)33, 1296–1316 (1935)

    Google Scholar 

  • Hallervordern, J.: Über eine Kohlenoxydvergiftung im Fetalleben mit Entwicklungsstörung der Hirnrinde. Allg. Z. Psychiat.124, 289–298 (1949)

    Google Scholar 

  • Halsey, J. H., Allen, N., Chamberlan, H. R.: The morphogenesis of hydranencephaly. J. neurol. Sci.12, 187–217 (1971)

    Google Scholar 

  • Huttenlocher, P. R.: Dendritic development in neocortex of children with mental defect and infantile spasms. Neurology (Minneap.)24, 203–210 (1974)

    Google Scholar 

  • Huttenlocher, P.: Synaptic and dendritic development and mental defect. In: Brain mechanisms in mental retardation (eds. N. A. Buchwald and M. A. B. Brazier), pp. 123–140. (UCLA Forum in Medical Sciences, No. 18.) New York: Academic Press 1975

    Google Scholar 

  • Jacob, H.: Die feine Oberflächengestaltung der Hirnwindungen: die Hirnwarzenbildung und Mikropolygyrie. Z. ges. Neurol. Psychiat.170, 64–84 (1940)

    Google Scholar 

  • Jones, E. G.: Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J. comp. Neurol.160, 205–268 (1975)

    Google Scholar 

  • Kölliker, A.: Handbuch der Gewebelehre des Menschen. Leipzig: Engelmann 1896

    Google Scholar 

  • Levine, D. N., Fisher, M. A., Caviness, V. S., Jr.: Porencephaly with microgyria: a Pathologic study. Acta neuropath. (Berl.)29, 99–113 (1974)

    Google Scholar 

  • Lim, R., Mitsunobo, K.: Brain cells in culture: morphological transformation by a protein. Science185, 63–66 (1974)

    Google Scholar 

  • Lorente de Nó: Studies on the structure of the cerebral cortex: I. Area entorhinalis. J. Psychol. Neurol. (Lpz.)45, 381–438 (1933)

    Google Scholar 

  • Lorente de Nó: Cerebral cortex: architecture, intracortical connections, major pro-jections. In: Physiology of the nervous system (ed. J. F. Fulton), Ed. 3. New York: Oxford Univ. Press 1949

    Google Scholar 

  • Lund, J. S.: Non-pyramidal cells of layers I–IV in the monkey striate cortex. Anat. Rec.166, 339 (1969)

    Google Scholar 

  • Lund, J. S.: Organization of neurons in the visual cortex, area 17, of the monkey, (macaca mulatta). J. comp. Neurol.147, 455–496 (1973) 197–205 (1971)

    Google Scholar 

  • Marin-Padilla, M.: Structural abnormalities of the cerebral cortex in human chromosomal aberrations: a Golgi study. Brain Res.44, 625–629 (1972)

    Google Scholar 

  • Marin-Padilla, M.: Structural organization of the cerebral cortex (motor area) in human chromsomal aberrations. A Golgi study. I. D. (13–15) trisomy, Patau syndrome. Brain Res.66, 375–391 (1974)

    Google Scholar 

  • Menser, M. A., Reye, R. D. K.: The pathology of congenital rubella. A review written by request. Pathology6, 215–222 (1974)

    Google Scholar 

  • 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 

  • Myers, R. E.: Brain pathology following fetal vascular occlusion: an experimental study. Invest. Ophthal.8, 41–50 (1969)

    Google Scholar 

  • Navin, J. J., Angevine, J. M.: Congenital cytomegalic inclusion disease with porencephaly. Neurology (Minneap.)18, 470–472 (1968)

    Google Scholar 

  • Nieuwenhuijse, P.: Zur Kenntnis der Mikrogyrie. Psychiat. neurol. Bl. (Amst.)17, 9–53 (1913)

    Google Scholar 

  • Norman, R. M.: Malformations of the nervous system, birth injury, and diseases of early life. In: Greenfield's neuropathology, Ed. 2, pp. 324–440 (ed. W. Blackwood et al.). Baltimore:Williams and Wilkins 1963

    Google Scholar 

  • Osburn, B. I., Silverstein, A. M., Prendergast, R. A., Johnson, R. T., Parshall, C. J.: Experimental viral induced congenital encephalopathies: I. Pathology of hydran-encephaly and porencephaly caused by bluetongue virus vaccine. Lab. Invest.25, 197–205 (1971)

    Google Scholar 

  • Poliakov, G. I.: Some results of research into the development of the neuronal structure of the cortical analyzers in man. J. comp. Neurol.117, 197–212 (1961)

    Google Scholar 

  • Poliakov, G. I.: Embryonal and postembryonal development of neurons of the human cerebral cortex. In: Evolution of the forebrain (eds. R. Hassler and H. Stephen), pp. 249–258. New York: Plenum Press 1967

    Google Scholar 

  • Poliakov, G. I.: Relations between some structural parameters of types and forms of neurons effecting different kinds of switches in the neocortex. J. Hirnforsch.15, 249–268 (1974)

    Google Scholar 

  • Purpura, D. P.: Dendritic spine “dysgenesis” and mental retardation. Science186, 1126–1128 (1974)

    Google Scholar 

  • Purpura, D. P.: Dendritic differentiation in human cerebral cortex: normal and aberrant developmental patterns. In: Physiology and pathology of dendrites (ed. G. W. Kreutzberg), pp. 91–116. New York: Raven Press 1975a

    Google Scholar 

  • Purpura, D. P.: Normal and aberrant neuronal development in the cerebral cortex of the human fetus and young infant. In: Brain mechanisms in metal retardation (UCLA forum in Medical Science, No. 18), (eds. N. A. Buchwald and M. A. B. Brazier), pp. 141–167. New York: Academic Press 1975b

    Google Scholar 

  • Purpura, D. P., Housepian, E. M.: Morphological and physiological properties of chronically isolated immature cortex. Exp. Neurol.4, 377–401 (1961)

    Google Scholar 

  • Richman, D. P., Stewart, R. M., Caviness, V. S., Jr.: Cerebral microgyria in a 27 week fetus: an architectonic and topographic analysis. J. Neuropath. exp. Neurol.33, 374–384 (1974)

    Google Scholar 

  • Richman, D. P., Stewart, R. M., Hutchinson, J. W., Caviness, V. S., Jr.: Mechanical model of brain convolutional development. Science189, 18–21 (1975)

    Google Scholar 

  • Rutledge, L. T., Duncan, J., Cant, N.: Long term status of pyramidal cell axon collaterals and apical dendritic spines in denervated cortex. Brain Res.41, 249–262 (1975)

    Google Scholar 

  • Schmechel, D. E., Rakic, P.: Evolution of radial glial cells in developing monkey telencephalon: a Golgi study. Anat. Rec.175, 436 (1973)

    Google Scholar 

  • Scholz, U.: Topistic lesions. In: Selective vulnerability of the brain to hypoxaemia (eds. J. P. Schadé and W. H. McMenemy), pp. 257–267. Oxford: Blackwell 1963

    Google Scholar 

  • Stewart, R. M., Richman, D. P., Caviness, V. S., Jr.: Lissencephaly and pachygyria: an architectonic and topographical analysis. Acta neuropath. (Berl.)31, 1–12 (1975)

    Google Scholar 

  • Sumi, S. M., Hager, H.: Electronmicroscopic study of the reaction of the newborn rat brain to injury. Acta neuropath. (Berl.)10, 324–335 (1968a)

    Google Scholar 

  • Sumi, S. M., Hager, H.: Electronmicroscopic features of an experimentally produced porencephalic cyst in the rat brain. Acta neuropath. (Berl.)10, 336–346 (1968b)

    Google Scholar 

  • Valverde, F.: Short axon neuronal subsystems in the visual cortex of the monkey. Int. J. Neurosci.1, 181–197 (1971)

    Google Scholar 

  • Vander Eecken, H. M.: The anastemoses between the leptomeningeal arteries of the brain. Springfield, Ill.: Ch. C. Thomas 1959

    Google Scholar 

  • Yakovlev, P. I.: Whole brain serial histological sections. In: Neuropathology, methods and diagnoses (ed. C. G. Tedeschi), pp. 371–378. Boston: Little Brown and Comp. 1970

    Google Scholar 

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This paper was read in part at the Fifty-First Annual Meeting of the American Association of Neuropathologists, New York, June 2, 1975.

This study was supported in part by USPHS grant H D 04147, Nationale Institute of Health, Bethesda and the Joseph P. Kennedy, Jr., Memorial Foundation.

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Williams, R.S., Ferrante, R.J. & Caviness, V.S. The cellular pathology of microgyria. Acta Neuropathol 36, 269–283 (1976). https://doi.org/10.1007/BF00685371

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