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Translational Neuroscience

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The discovery of the subpial granular layer in the human cerebral cortex

Miloš Judaš / Mihovil Pletikos
Published Online: 2010-09-29 | DOI: https://doi.org/10.2478/v10134-010-0037-4

Abstract

The subpial granular layer (SGL) is a transient accumulation of tangentially migrating small granular neurons in the marginal zone of the developing fetal neocortex. It has recently attracted attention as a possible additional source of future cortical interneurons, or even as a putative precursor pool for generation of Cajal-Retzius cells. The discovery of the SGL is generally attributed to Otto Ranke and it is usually claimed that the SGL is specific for human brain. The aim of this review is: (1) to demonstrate that the first to observe SGL in the human cerebral cortex was not Otto Ranke in 1910, but Franz Boll in 1874; (2) to provide an English translation of Ranke’s original description of the SGL and thus demonstrate that he described the SGL in both human and animal brain; and (3) to provide a concise review of current studies concerning the developmental fate and possible functions of the transient fetal SGL.

Keywords: Subpial granular layer; Marginal zone; Developing neocortex; Otto Ranke; Franz Boll

  • [1] Brun A (1965) The subpial granular layer of the foetal cerebral cortex in man. Acta Pathol Microbiol Scand (Suppl 179) 13:1–98 Google Scholar

  • [2] Gadisseux JF, Goffinet AM, Lyon G, Evrard P (1992) The human transient subpial granular layer: An optical, immunohistochemical, and ultrastructural analysis. J Comp Neurol 324:94–114 http://dx.doi.org/10.1002/cne.903240108CrossrefGoogle Scholar

  • [3] Sidman RL, Rakic P (1982) Development of the human central nervous system. In: Haymaker W, Adams RD (Eds) Histology and Histopathology of the Nervous System. Springfield: C.C. Thomas, pp. 3–145 Google Scholar

  • [4] Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9:110–122 http://dx.doi.org/10.1038/nrn2252Web of ScienceCrossrefGoogle Scholar

  • [5] Rakic P (2009) Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci 10:724–735 http://dx.doi.org/10.1038/nrn2719CrossrefWeb of ScienceGoogle Scholar

  • [6] Ranke O (1910) Beiträge zur Kenntnis der normalen und pathologischen Hirnrindenbildung. Beitr Pathol Anat Allgem Pathol 47(1):51–125 Google Scholar

  • [7] Boll F (1874) Die Histiologie und Histiogenese der nervösen Centralorgane. Arch Psychiatr Nervenkr 4:1–138 http://dx.doi.org/10.1007/BF02346085CrossrefGoogle Scholar

  • [8] Hess N (1858) De Cerebelli Gyrorum Textura Disquisitiones Microscopicae. Dissertatio inauguralis. Tartu (Russia): Schünmann & Mattiesen, 36pp Google Scholar

  • [9] Ranke O (1908) Ueber Gehirnveränderungen bei der angeborenen Syphilis. Habilitationsschrift zur Erlangung der venia legendi einer hohen medizinischen Fakultät der Ruprecht-Karls-Universität zu Heidelberg vorgelegt von Dr. Otto Ranke, Assistent an der psychiatrischen Klinik. Jena, Gustav Fischer, 97pp Google Scholar

  • [10] Judaš M, Sedmak G, Pletikos M (2010) early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974). J Anat (Lond) 217:344–367 Web of ScienceGoogle Scholar

  • [11] Schaffer K (1917) Ueber normale und pathologische Hirnfurchung. Z Ges Neurol Psychiat 38:1–34 http://dx.doi.org/10.1007/BF02871773CrossrefGoogle Scholar

  • [12] Filimonoff IN (1929) Zur embryonalen und postembryonalen Entwicklung der Grosshirnrinde des Menschen. J Psychol Neurol (Leipzig) 39:323–389 Google Scholar

  • [13] Poljakow GI (1979) Entwicklung der Neuronen der menschlichen Grosshirnrinde (Herausgegeben von B. Schönheit). Leipzig: VEB Georg Thieme, 320pp Google Scholar

  • [14] Sanides F, Sas E (1970) Persistence of horizontal cells of the Cajal foetal type and of the subpial granular layer in parts of the mammalian paleocortex (with 10 figures). Ztschr Mikr-Anat Forschung 82:570–588 Google Scholar

  • [15] Zečević N, Rakic P (2001) Development of layer I neurons in the primate cerebral cortex. J Neurosci 21(15):5607–5619 PubMedGoogle Scholar

  • [16] Meyer G, Soria JM, Martínez-Galán JR, Martín-Clemente B, Fairén A (1998) Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol 397:493–518 http://dx.doi.org/10.1002/(SICI)1096-9861(19980810)397:4<493::AID-CNE4>3.0.CO;2-XCrossrefGoogle Scholar

  • [17] Jiménez D, Rivera R, López-Mascaraque L, De Carlos JA (2003) Origin of the cortical layer I in rodents. Dev Neurosci 25:105–115 http://dx.doi.org/10.1159/000072260CrossrefGoogle Scholar

  • [18] Meyer G, Wahle P (1999) The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the fetal human neocortex. Eur J Neurosci 11:3937–3944 http://dx.doi.org/10.1046/j.1460-9568.1999.00818.xCrossrefGoogle Scholar

  • [19] Meyer G, Goffinet AM, Fairén A (1999) What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cereb Cortex 9:765–775 http://dx.doi.org/10.1093/cercor/9.8.765CrossrefGoogle Scholar

  • [20] Bielschowsky M (1923) Ueber die Oberflächengestaltung des Grosshirnmantels bei Pachygyrie, Microgyrie und bei normaler Entwicklung. J Psychol Neurol 30:29–76 Google Scholar

  • [21] Rakic P, Sidman RL (1968) Supravital DNA synthesis in the developing human and mouse brain. J Neuropathol Exp Neurol 27:246–276 http://dx.doi.org/10.1097/00005072-196804000-00006CrossrefGoogle Scholar

  • [22] Evrard P, De Saint-Georges P, Kadhim H, Gadisseux JF (1989) In: French JH, Hard S, Casaer P (Eds) Pathology of Prenatal Encephalopathies in Childhood Neurology and Developmental Disabilities. Baltimore: Paul H. Brookes Publishing Co., pp. 153–176 Google Scholar

  • [23] Spreafico R, Arcelli P, Frassoni C, Canetti P, Giaccone G, Rizzuti T, Mastrangelo M, Bentivoglio M (1999) Development of layer I of the human cerebral cortex after midgestation: Architectonic fundings, immunocytochemical identification of neurons and glia, and in situ labeling of apoptotic cells. J Comp Neurol 410:126–142 http://dx.doi.org/10.1002/(SICI)1096-9861(19990719)410:1<126::AID-CNE11>3.0.CO;2-5CrossrefGoogle Scholar

  • [24] Larroche JC (1981) The marginal layer in the neocortex of a 7 weekold human embryo. A light and electron microscopic study. Anat Embryol 162:301–312 http://dx.doi.org/10.1007/BF00299974CrossrefGoogle Scholar

  • [25] Marin-Padilla M (1983) Structural organization of the human cerebral cortex prior to the appearance of the cortical plate. Anat Embryol 168:21–40 http://dx.doi.org/10.1007/BF00305396CrossrefGoogle Scholar

  • [26] Zečević N (1993) Cellular composition of the telencephalic wall in human embryos. Early Hum Dev 32:131–149 http://dx.doi.org/10.1016/0378-3782(93)90007-HCrossrefGoogle Scholar

  • [27] Zečević N, Milošević A, Rakic S, Marin-Padilla M (1999) Early development and composition of the human primordial plexiform layer: an immunohistochemical study. J Comp Neurol 412:241–254 http://dx.doi.org/10.1002/(SICI)1096-9861(19990920)412:2<241::AID-CNE5>3.0.CO;2-XCrossrefGoogle Scholar

  • [28] Meyer G, Schaaps JP, Moreau L, Goffinet AM (2000) Embryonic and early fetal development of the human neocortex. J Neurosci 20:1858–1868 Google Scholar

  • [29] Meyer G, Perez-Garcia CG, Abraham H, Caput D (2002b) Expression of p73 and reelin in the developing human cortex. J Neurosci 15:22:4973–4986 Google Scholar

  • [30] Meyer G, Lambert de Rouvroit C, Goffinet AM, Wahle P (2003) Disabled-1 mRNA and protein expression in developing human cortex. Eur J Neurosci 17:517–525 http://dx.doi.org/10.1046/j.1460-9568.2003.02480.xCrossrefGoogle Scholar

  • [31] Bystron I, Molnár Z, Otellin V, Blakemore C (2005) Tangential networks of precocious neurons and early axonal outgrowth in the embryonic human forebrain. J Neurosci 25:2781–2792 http://dx.doi.org/10.1523/JNEUROSCI.4770-04.2005CrossrefGoogle Scholar

  • [32] Bystron I, Rakic P, Molnár Z, Blakemore C (2006) The first neurons of the human cerebral cortex. Nat Neurosci 9:880–886 http://dx.doi.org/10.1038/nn1726CrossrefGoogle Scholar

  • [33] Zečević N, Milošević A (1997) Initial development of g-aminobutyric acid immunoreactivity in the human cerebral cortex. J Comp Neurol 380:495–506 http://dx.doi.org/10.1002/(SICI)1096-9861(19970421)380:4<495::AID-CNE6>3.0.CO;2-XCrossrefGoogle Scholar

  • [34] Meyer G, Goffinet AM (1998) Prenatal development of reelinimmunoreactive neurons in the human neocortex. J Comp Neurol 397:29–40 http://dx.doi.org/10.1002/(SICI)1096-9861(19980720)397:1<29::AID-CNE3>3.0.CO;2-KCrossrefGoogle Scholar

  • [35] Marin-Padilla M (1995) Prenatal development of fibrous (white matter), protoplasmic (gray matter), and layer I astrocytes in the human cerebral cortex: A Golgi study. J Comp Neurol 357:554–572 http://dx.doi.org/10.1002/cne.903570407CrossrefGoogle Scholar

  • [36] Meyer G, Gonzalez-Hernandez T (1993) Developmental changes in layer I of the human neocortex during prenatal life: A DiI-tracing and AChE and NADPH-d histochemistry study. J Comp Neurol 338:317–336 http://dx.doi.org/10.1002/cne.903380302CrossrefGoogle Scholar

  • [37] Rakic S, Zečević N (2003) Emerging complexity of layer I in human cerebral cortex. Cereb Cortex 13:1072–1083 http://dx.doi.org/10.1093/cercor/13.10.1072CrossrefGoogle Scholar

  • [38] 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 http://dx.doi.org/10.1007/BF00318504CrossrefGoogle Scholar

  • [39] Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian forebrain. Development 128:3759–3771 Google Scholar

  • [40] Meyer G, Perez-Garcia CG, Gleeson JG (2002a) Selective expression of doublecortin and LIS1 in developing human cortex suggests unique modes of neuronal movement. Cereb Cortex 12:1225–1236 http://dx.doi.org/10.1093/cercor/12.12.1225Google Scholar

  • [41] Kostović I, Judaš M, Kostović-Knežević’ Lj, Šimić G, Delalle I, Chudy D, Šajin B, Petanjek Z (1991) Zagreb Research Collection of human brains for developmental neurobiologists and clinical neuroscientists. Int J Dev Biol 35:215–230 PubMedGoogle Scholar

  • [42] Kostović I, Jovanov-Milošević N, Krsnik Ž, Petanjek Z, Judaš M (2004) Laminar organization of the marginal zone in the human fetal cortex. Neuroembryology 3:19–26 http://dx.doi.org/10.1159/000085401CrossrefGoogle Scholar

About the article

Published Online: 2010-09-29

Published in Print: 2010-09-01


Citation Information: Translational Neuroscience, Volume 1, Issue 3, Pages 255–260, ISSN (Online) 2081-6936, ISSN (Print) 2081-3856, DOI: https://doi.org/10.2478/v10134-010-0037-4.

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© 2010 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

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