Neocortical histogenesis in normal and reeler mice: A developmental study based upon [3H]thymidine autoradiography
Abstract
The relative positions of the principal neuronal classes of neocortex are inverted in the reeler mutant mouse. Neurons formed at 48-hourly intervals throughout the period of neocortical cytogenesis between E11 and E17 are labeled by [3H]thymidine. The positions of the labeled cells during and subsequent to their migrations are traced by autoradiography. Simultaneously-formed cohorts reach the neocortex at the same time in normal and reeler animals. After E13, subsequent to the appearance of the cortical plate, cohorts of migrating cells in the normal animal ascend to the interface of the cortical plate and marginal layer where they come to rest in a narrow laminar zone. In reeler, by contrast, migration is arrested in the depths of the cortex. The migrating cell appears unable to ascend through the zone occupied by the preceding cohorts. At the completion of migration neurons of both genotypes become fixed in position and undergo little subsequent shift in their relative positions in the course of future cortical growth. Despite the anomaly of migrations and the post-migratory positions of neurons in reeler, cohorts of cells formed at the same time in the two genotypes give rise to the same neuronal classes.
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The reeler mouse mutant has neurons generated normally but abnormally placed, resulting in disorganization of cortical laminar layers in the CNS.
“The reeler is an autosomal recessive mouse mutant, in which neurons are generated normally but are abnormally placed, resulting in disorganization of cortical laminar layers in the CNS (7–12).”
From Reelin molecules assemble together to form a large protein complex, which is inhibited by the function-blocking CR-50 antibody (2000) · cites this paper as [10]
In the reeler mouse model, lamination of principal cells in cortex is inverted and the s.p. of the hippocampus is split in region CA1.
“in the reeler mouse model, in which expression of reelin or associated proteins is disrupted, the lamination of PCs in cortex is inverted and the s.p. of the hippocampus is split in region CA1”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [178]
Cites
Mode of cell migration to the superficial layers of fetal monkey neocortex
Rakic, P. (1972) · Journal of Comparative Neurology · doi:10.1002/cne.901450105 · Cited by 2,170 · see citing works
Autoradiographic Study of Cell Migration during Histogenesis of Cerebral Cortex in the Mouse
ANGEVINE, J. B., & SIDMAN, R. L. (1961) · Nature · doi:10.1038/192766b0 · Cited by 1,530 · see citing works
Physiological and Biochemical Aspects of Nervous Integration
Carlson, F. D. (1968) · Cited by 749 · see citing works
Schmechel, D. E., & RAKIC, P. T. (1979) · Anatomy and Embryology · doi:10.1007/bf00300010 · Cited by 676 · see citing works
The migration of neuroblasts in the developing cerebral cortex.
Berry, M., & Rogers, A. W. (1965) · PubMed · Cited by 675 · see citing works
Mechanisms of Cortical Development: A View From Mutations in Mice
Caviness, V. S., & RAKIC, P. T. (1978) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.01.030178.001501 · Cited by 653 · see citing works
Self-citationThe ‘module-concept’ in cerebral cortex architecture
Szentágothai, J. (1975) · Brain Research · doi:10.1016/0006-8993(75)90122-5 · Cited by 614 · see citing works
Falconer, D. S. (1951) · Journal of Genetics · doi:10.1007/bf02996215 · Cited by 539 · see citing works
Dual origin of the mammalian neocortex and evolution of the cortical plate
Marín‐Padilla, M. (1978) · Anatomy and Embryology · doi:10.1007/bf00315920 · Cited by 508 · see citing works
Architectonic map of neocortex of the normal mouse
Caviness, V. S. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901640207 · Cited by 448 · see citing works
Self-citationCell migrations to the isocortex in the rat
Hicks, S. P., & D’Amato, C. J. (1968) · The Anatomical Record · doi:10.1002/ar.1091600311 · Cited by 417 · see citing works
Caviness, V. S., & Sidman, R. L. (1973) · Journal of Comparative Neurology · doi:10.1002/cne.901480202 · Cited by 413 · see citing works
Self-citationLevitt, P. R., Cooper, M., & RAKIC, P. T. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-01-00027.1981 · Cited by 395 · see citing works
Autoradiographic Methods and Principles for Study of the Nervous System with Thymidine-H3
Sidman, R. L. (1970) · Springer eBooks · doi:10.1007/978-3-642-85986-1_12 · Cited by 312 · see citing works
Shoukimas, G. M., & Hinds, J. W. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901790407 · Cited by 280 · see citing works
Frontiers in neurology and neuroscience research
Brown, G. (1973) · Physiology & Behavior · doi:10.1016/0031-9384(73)90364-8 · Cited by 269 · see citing works
Development of the barrels and barrel field in the somatosensory cortex of the mouse
Rice, F. L., & der Loos, H. V. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710408 · Cited by 264 · see citing works
Patterns of cell and fiber distribution in the neocortex of the reeler mutant mouse
Caviness, V. S. (1976) · The Journal of Comparative Neurology · doi:10.1002/cne.901700404 · Cited by 221 · see citing works
Self-citationCongenital and acquired cognitive disorders
Comings, D. E. (1979) · Europe PMC (PubMed Central) · Cited by 199 · see citing works
RAKIC, P. T., Stensaas, L. J., Sayre, E. P., & Sidman, R. L. (1974) · Nature · doi:10.1038/250031a0 · Cited by 185 · see citing works
Cell proliferation, migration and differentiation in the cerebral cortex of the golden hamster
Shimada, M., & Langman, J. (1970) · The Journal of Comparative Neurology · doi:10.1002/cne.901390206 · Cited by 172 · see citing works
Lord, M., & Caviness, V. S. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870104 · Cited by 163 · see citing works
Self-citationTiming of Major Ontogenetic Events in the Visual Cortex of the Rhesus Monkey
RAKIC, P. T. (1975) · Elsevier eBooks · doi:10.1016/b978-0-12-139050-1.50008-2 · Cited by 154 · see citing works
The cortical plate and molecular layer of the late rat fetus
Peters, A., & Feldman, M. (1973) · Zeitschrift f�r Anatomie und Entwicklungsgeschichte · doi:10.1007/bf00523363 · Cited by 148 · see citing works
Caviness, V. S., So, D., & Sidman, R. L. (1972) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a108286 · Cited by 129 · see citing works
Self-citationBrain mechanisms in mental retardation
Spehlmann, R. (1976) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(76)90016-x · Cited by 124 · see citing works
Dynamical aspects of neocortical histogenesis in the rat
Raedler, E., Raedler, A., & Feldhaus, S. (1980) · Anatomy and Embryology · doi:10.1007/bf00301816 · Cited by 103 · see citing works
Lemmon, V., & Pearlman, A. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-01-00083.1981 · Cited by 92 · see citing works
Observations on the organization of the visual cortex in the reeler mouse
Dräger, U. C. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.902010407 · Cited by 76 · see citing works
Early cortical histogenesis in the primary olfactory cortex of the mouse
Derer, P., Caviness, V. S., & Sidman, R. L. (1977) · Brain Research · doi:10.1016/0006-8993(77)90641-2 · Cited by 59 · see citing works
Self-citationAutoradiographic Study of Development of the Cerebral Cortex in the Rabbit
Fernández, V., & Bravo, H. (2008) · Brain Behavior and Evolution · doi:10.1159/000123674 · Cited by 59 · see citing works
Caviness, V. S., & Korde, M. G. (1981) · Brain Research · doi:10.1016/0006-8993(81)91167-7 · Cited by 51 · see citing works
Self-citationRadial neuronal assemblies, ectopia and necrosis of developing cortex: A case analysis
Caviness, V. S., Evrard, P., & Lyon, G. (1978) · Acta Neuropathologica · doi:10.1007/bf00689559 · Cited by 48 · see citing works
Self-citationDerer, P. (1979) · Neuroscience Letters · doi:10.1016/0304-3940(79)90041-7 · Cited by 33 · see citing works
Reeler Mutant Mice and Laminar Distribution of Afferents in the Neocortex
Caviness, V. S. (1976) · Springer eBooks · doi:10.1007/978-3-642-81055-8_47 · Cited by 26 · see citing works
Self-citationCellular pathology of developing human cortex.
Vs, C., & Rs, W. (1979) · PubMed · Cited by 25 · see citing works
Reeler Mutant Mice: Physiology in Primary Visual Cortex
Dräger, U. C. (1976) · Springer eBooks · doi:10.1007/978-3-642-81055-8_48 · Cited by 19 · see citing works
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Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · see citing works
Linked Regularities in the Development and Evolution of Mammalian Brains
Finlay, B. L., & Darlington, R. B. (1995) · Science · doi:10.1126/science.7777856 · Cited by 1,217 · see citing works
Translating developmental time across mammalian species
Clancy, B., Darlington, R. B., & Finlay, B. L. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00171-3 · Cited by 1,221 · see citing works
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Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · see citing works
Ogawa, M., Miyata, T., Nakajimat, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., & Mikoshibat, K. (1995) · Neuron · doi:10.1016/0896-6273(95)90329-1 · Cited by 889 · see citing works
Tbr1 regulates differentiation of the preplate and layer 6
Hevner, R. F., Shi, L., Justice, N., Hsueh, Y.-P., Sheng, M., Smiga, S., Bulfone, A., Goffinet, A. M., Campagnoni, A. T., & Rubenstein, J. L. R. (2001) · Neuron · doi:10.1016/s0896-6273(01)00211-2 · Cited by 857 · see citing works
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687 · see citing works
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Rice, D. S., & Curran, T. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1005 · Cited by 667 · see citing works
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Dehay, C., & Kennedy, H. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2097 · Cited by 655 · see citing works
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Herz, J., & Chen, Y. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2009 · Cited by 524 · see citing works
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Barros, C. S., Franco, S. J., & Muller, U. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005108 · Cited by 506 · see citing works
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Marin, O., Valiente, M., Ge, X., & Tsai, L.-H. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001834 · Cited by 417 · see citing works
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Rice, D. S., Sheldon, M., D’Arcangelo, G., Nakajima, K., Goldowitz, D., & Curran, T. (1998) · Development · doi:10.1242/dev.125.18.3719 · Cited by 378 · see citing works
Cortical development: View from neurological mutants two decades later
Rakic, P., & Caviness, V. S. (1995) · Neuron · doi:10.1016/0896-6273(95)90258-9 · Cited by 287 · see citing works
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Makris, N., Buka, S. L., Biederman, J., Papadimitriou, G. M., Hodge, S. M., Valera, E. M., Brown, A. B., Bush, G., Monuteaux, M. C., Caviness, V. S., et al. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm156 · Cited by 239 · see citing works
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Hevner, R. F., Daza, R. A. M., Englund, C., Kohtz, J., & Fink, A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.11.033 · Cited by 180 · see citing works
Essential roles for the splicing regulator nSR100/SRRM4 during nervous system development
Quesnel-Vallières, M., Irimia, M., Cordes, S. P., & Blencowe, B. J. (2015) · Genes & Development · doi:10.1101/gad.256115.114 · Cited by 155 · see citing works
Fairén, A., Cobas, A., & Fonseca, M. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902510105 · Cited by 158 · see citing works
Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling
Pla, R., Borrell, V., Flames, N., & Marín, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0245-06.2006 · Cited by 151 · see citing works
Differential survival of Cajal-Retzius cells in organotypic cultures of hippocampus and neocortex
Del Rı́o, J. A., Heimrich, B., Supèr, H., Borrell, V., Frotscher, M., & Soriano, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-21-06896.1996 · Cited by 133 · see citing works
Utsunomiya-Tate, N., Kubo, K.-I., Tate, S.-I., Kainosho, M., Katayama, E., Nakajima, K., & Mikoshiba, K. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.160272497 · Cited by 131 · see citing works
Miller, B., Sheppard, A. M., Bicknese, A. R., & Pearlman, A. L. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903550410 · Cited by 114 · see citing works
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Herring, A., Donath, A., Steiner, K. M., Widera, M. P., Hamzehian, S., Kanakis, D., Kölble, K., ElAli, A., Hermann, D. M., Paulus, W., et al. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2012-112069 · Cited by 92 · see citing works
Inoue, T., Ogawa, M., Mikoshiba, K., & Aruga, J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5735-07.2008 · Cited by 76 · see citing works
Alcántara, S., Pozas, E., Ibañez, C. F., & Soriano, E. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhi128 · Cited by 71 · see citing works
Soumiya, H., Fukumitsu, H., & Furukawa, S. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22704 · Cited by 58 · see citing works
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Cremer, C. M., Lübke, J. H. R., Palomero-Gallagher, N., & Zilles, K. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0303-3 · Cited by 17 · see citing works
- Authors
- Caviness, V. S.
- Affiliations
- Harvard University (US)
- Corresponding author
- Caviness, Verne S.
- Venue
- Developmental Brain Research
- Publisher
- Elsevier BV
- Published
- 1982-07
- Volume
- 4
- Issue
- 3
- Pages
- 293-302
- ISSN
- 0165-3806 (ISSN-L)
- OpenAlex
- W1979060895
- Cited by
- 639
- References
- 37
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 12 · 2023: 6 · 2022: 11 · 2021: 11 · 2020: 10 · 2019: 6 · 2018: 6 · 2017: 12 · 2016: 12 · 2015: 11 · 2014: 11 · 2013: 13 · 2012: 25
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS012005)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Keywords
- neuronal migration, cortical lamination, cortical plate, cortical development, 3H-thymidine labeling
- MeSH terms
- Animals, Autoradiography, Cerebral Cortex, DNA Replication, Female, Mice, Inbred Strains, Mice, Neurologic Mutants, Pregnancy, Species Specificity, Thymidine, Mice
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