Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory
Abstract
The prenatal development of the mammalian neocortex has been analyzed, with the rapid Golgi method, in a variety of experimental animals (hamster, mouse, rat, and cat) and in humans. A new developmental conception of the structural organization of the mammalian neocortex is discussed. Neocortical development begins with the establishment of the primordial plexiform layer (PPL) which precedes and is a prerequisite for the subsequent formation of the cortical plate (CP). The formation of the CP occurs, in its entirety, within the PPL. During its development, three fundamental neuronal events occur: migration, early differentiation, and late maturation. All migrating neurons, travelling on radial glial fibers, reach layer I, develop an apical dendrite, and establish contacts with its elements. These newly differentiated neurons assume similar morphology resembling embryonic pyramidal cells. As such, an early differentiation stage common to all neurons of the CP is established. During the late maturation stage, all CP neurons acquire their specific phenotypic structural and functional features. Only pyramidal neurons retain and expand their original connections with layer I while other neuronal types lose these connections. The pyramidal cell is redefined in developmental terms: the neocortex's pyramidal cell is both structurally and functionally locked into position between layer I and the cortical depth of its soma. During mammalian evolution pyramidal cells are forced to structurally and functionally elongate their apical dendrite outwardly to accommodate an increasing amount of information without losing either their original anchorage to layer I or their cortical depth. This unique property of pyramidal neurons is considered to be a mammalian innovation. Based on these observations, a unifying developmental cytoarchitectonic theory applicable to all mammals is proposed. The theory considers the CP to be a mammalian innovation and to represent a single, stratified, and expanding telencephalic nucleus. The theory envisions the mammalian neocortex as an open biological system capable of progressive expansion by the recruitment and transformation of primitive neurons from upper layer II into pyramidal cells. Hence, the number of pyramidal cell strata increases over the course of mammalian phylogeny. The developmental roles of layer I in the migration of neurons, formation of the CP, unique morphology of pyramidal cells, and overall structural organization of the mammalian neocortex are emphasized.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Layers 2 and 3 in human and other primates are greatly expanded compared to mouse, suggesting a substantially increased intracortical connectivity in human.
“Layers 2 and 3 in human and other primates are greatly expanded compared to mouse, suggesting the occurrence of a substantially increased intracortical connectivity in human (Marin-Padilla, 1992).”
From Large-Scale Cellular-Resolution Gene Profiling in Human Neocortex Reveals Species-Specific Molecular Signatures (2012) · cites this paper as Marin-Padilla, 1992
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
Estes, R., & Romer, A. S. (1967) · Copeia · doi:10.2307/1441916 · Cited by 1,212 · see citing works
The Structure and Function of Nervous Tissue
(1972) · Elsevier eBooks · doi:10.1016/b978-0-12-119284-6.x5001-5 · Cited by 914 · see citing works
Kostović, I., & RAKIC, P. T. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970309 · Cited by 912 · see citing works
THE BASIC UNIFORMITY IN STRUCTURE OF THE NEOCORTEX
Röckel, A., Hiorns, R. W., & Powell, T. P. S. (1980) · Brain · doi:10.1093/brain/103.2.221 · Cited by 902 · see citing works
Bergen, D. C. (1988) · JAMA · doi:10.1001/jama.1988.03410010112050 · Cited by 665 · see citing works
Subplate Neurons Pioneer the First Axon Pathway from the Cerebral Cortex
McConnell, S. K., Ghosh, A., & Shatz, C. J. (1989) · Science · doi:10.1126/science.2475909 · Cited by 647 · see citing works
The Brain of the Tiger Salamander.
Crosly, E. C., & Herrick, C. J. (1949) · The American Midland Naturalist · doi:10.2307/2422029 · Cited by 566 · see citing works
Nowack, W. J. (1989) · Neurology · doi:10.1212/wnl.39.9.1274-a · Cited by 533 · 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
Self-citationKostović, I., & RAKIC, P. T. (1980) · Journal of Neurocytology · doi:10.1007/bf01205159 · Cited by 499 · see citing works
Luskin, M., & Shatz, C. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-04-01062.1985 · Cited by 493 · see citing works
Physiology of the Nervous System
&NA; (1950) · Academic Medicine · doi:10.1097/00001888-195005000-00043 · Cited by 492 · see citing works
Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans
RAKIC, P. T., & Sidman, R. L. (1970) · The Journal of Comparative Neurology · doi:10.1002/cne.901390407 · Cited by 412 · see citing works
Wilson, S. W., Ross, L. S., Parrett, T. J., & Easter, S. S. (1990) · Development · doi:10.1242/dev.108.1.121 · Cited by 408 · see citing works
The Human Brain in Figures and Tables
Snider, R. S. (1969) · Neurology · doi:10.1212/wnl.19.7.714-a · Cited by 400 · see citing works
Marín‐Padilla, M. (1971) · Anatomy and Embryology · doi:10.1007/bf00519296 · Cited by 385 · see citing works
Self-citationHendelman, W. J. (1992) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1992.4.2.175 · Cited by 364 · see citing works
Cáceres, A., Binder, L., Payne, M., Bender, P. K., Rebhun, L. I., & Steward, O. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-02-00394.1984 · Cited by 352 · see citing works
Signal and sense : local and global order in perceptual maps
Edelman, G. M., Gall, W. E., & Cowan, W. M. (1990) · Cited by 337 · see citing works
The matrix cell and cytogenesis in the developing central nervous system
Fujita, S. (1963) · The Journal of Comparative Neurology · doi:10.1002/cne.901200104 · Cited by 328 · see citing works
(1984) · Cerebral cortex · doi:10.1007/978-1-4615-6610-6 · Cited by 289 · see citing works
Architectonics of the cerebral cortex
Powell, T. P. S. (1979) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(79)90162-x · Cited by 286 · see citing works
Marín‐Padilla, M. (1970) · Brain Research · doi:10.1016/0006-8993(70)90037-5 · Cited by 280 · see citing works
Self-citationShoukimas, G. M., & Hinds, J. W. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901790407 · Cited by 280 · see citing works
Initial expression and endogenous activation of NMDA channels in early neocortical development
LoTurco, J. J., Blanton, M. G., & Kriegstein, A. R. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-03-00792.1991 · Cited by 259 · see citing works
Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study
Mrzljak, L., Uylings, H. B. M., Kostović, I., & van Eden, C. G. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902710306 · Cited by 249 · see citing works
Chapter 9 Neuronal development in human prefrontal cortex in prenatal and postnatal stages
Mrzljak, L., Uylings, H. B. M., Van Eden, G. G., & Judáš, M. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62681-3 · Cited by 247 · see citing works
Development of Projection and Local Circuit Neurons in Neocortex
Miller, M. W. (1988) · Cerebral cortex · doi:10.1007/978-1-4615-6619-9_5 · Cited by 246 · see citing works
Development of layer I and the subplate in the rat neocortex
Bayer, S. A., & Altman, J. (1990) · Experimental Neurology · doi:10.1016/0014-4886(90)90062-w · Cited by 237 · see citing works
Organization of pyramidal neurons in area 17 of monkey visual cortex
Peters, A., & Sethares, C. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903060102 · Cited by 212 · see citing works
The Role of the Subplate in the Development of the Mammalian Telencephalon
Shatz, C. J., Chun, J. J. M., & Luskin, M. B. (1988) · Cerebral cortex · doi:10.1007/978-1-4615-6619-9_2 · Cited by 192 · see citing works
Cellular components of the cerebral cortex
Peters, A., & Jones, E. G. (1984) · Plenum Press eBooks · Cited by 190 · see citing works
Origin of the pericellular baskets of the pyramidal cells of the human motor cortex: A golgi study
Marín‐Padilla, M. (1969) · Brain Research · doi:10.1016/0006-8993(69)90204-2 · Cited by 186 · see citing works
Self-citationA COMPARISON OF PRIMITIVE FOREBRAIN ORGANIZATION IN METATHERIAN AND EUTHERIAN MAMMALS*
Ebner, F. F. (1969) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1969.tb20447.x · Cited by 183 · see citing works
Structure and function of the nervous system
Simonsen, T. (2006) · Routledge eBooks · doi:10.1201/b13638-18 · Cited by 170 · see citing works
Marín‐Padilla, M., & Marin‐Padilla, T. M. (1982) · Anatomy and Embryology · doi:10.1007/bf00318504 · Cited by 168 · see citing works
Self-citationMarín‐Padilla, M. (1972) · Anatomy and Embryology · doi:10.1007/bf00519174 · Cited by 165 · see citing works
Self-citationEarly vascularization of the embryonic cerebral cortex: Golgi and electron microscopic studies
Marín‐Padilla, M. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902410210 · Cited by 159 · see citing works
Self-citationFairén, A., Cobas, A., & Fonseca, M. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902510105 · Cited by 158 · see citing works
Marín‐Padilla, M. (1970) · Brain Research · doi:10.1016/0006-8993(70)90038-7 · Cited by 157 · see citing works
Self-citationThe Cerebral Cortex of Reptiles
Ulinski, P. S. (1990) · Cerebral cortex · doi:10.1007/978-1-4757-9622-3_5 · Cited by 150 · see citing works
Cell migration in the rat embryonic neocortex
Bayer, S. A., Altman, J., Russo, R. J., Dai, X., & Simmons, J. A. T. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903070312 · Cited by 147 · see citing works
The onset of synaptogenesis in rat temporal cortex
K�nig, N., Roch, G., & Marty, R. (1975) · Anatomy and Embryology · doi:10.1007/bf00315564 · Cited by 143 · see citing works
The Growth and Development of Microvasculature in Human Cerebral Cortex
Norman, M. G., & OʼKusky, J. R. (1986) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-198605000-00003 · Cited by 129 · see citing works
Early Ontogenesis of the Human Cerebral Cortex
Marín‐Padilla, M. (1988) · Cerebral cortex · doi:10.1007/978-1-4615-6619-9_1 · Cited by 129 · see citing works
Self-citationA RATIONAL SUBDIVISION OF THE CEREBRAL CORTEX
Filimonoff, I. N. (1947) · Archives of Neurology And Psychiatry · doi:10.1001/archneurpsyc.1947.02300320047002 · Cited by 126 · see citing works
Three‐dimensional structural organization of layer I of the human cerebral cortex: A golgi study
Marín‐Padilla, M. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902990107 · Cited by 124 · see citing works
Self-citationStructural organization of the human cerebral cortex prior to the appearance of the cortical plate
Marín‐Padilla, M. (1983) · Anatomy and Embryology · doi:10.1007/bf00305396 · Cited by 118 · see citing works
Self-citationOn the early development of the isocortex in fetal sheep.
Ke, A. (1967) · PubMed · Cited by 111 · see citing works
Intrinsic neocortical organization: Some comparative aspects
Valverde, F. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90174-0 · Cited by 108 · see citing works
Morphology of the Developing Visual Cortex of the Human Infant
Takashima, S., Chan, F.-W., Becker, L. E., & ARMSTRONG, D. L. (1980) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-198007000-00007 · Cited by 108 · see citing works
Glial and Neuronal Cell Biology
(1982) · Archives of Neurology · doi:10.1001/archneur.1982.00510200074022 · Cited by 107 · see citing works
Number and distribution of the apical dendritic spines of the layer V pyramidal cells in man
Marín‐Padilla, M. (1967) · The Journal of Comparative Neurology · doi:10.1002/cne.901310407 · Cited by 106 · see citing works
Self-citationDynamical 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
Forms and spatial arrangement of neurons in the primary motor cortex of man
Meyer, G. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902620306 · Cited by 97 · see citing works
The ?extraverted neurons? of the mammalian cerebral cortex
Sanides, F., & Sanides, D. (1972) · Anatomy and Embryology · doi:10.1007/bf00522616 · Cited by 94 · see citing works
The Pallium of Anuran Amphibians
Neary, T. J. (1990) · Cerebral cortex · doi:10.1007/978-1-4757-9622-3_4 · Cited by 88 · see citing works
The time of origin of Cajal-Retzius cells in the rat temporal cortex. An autoradiographic study
König, N., Valat, J., Fulcrand, J., & Marty, R. (1977) · Neuroscience Letters · doi:10.1016/0304-3940(77)90118-5 · Cited by 88 · see citing works
Neurons and Interneuronal Connections of the Central Visual System
Shkol’nik-Yarros, E. G. (1971) · Springer eBooks · doi:10.1007/978-1-4684-0715-0 · Cited by 86 · see citing works
Poli︠a︡kov, G. I. (1961) · The Journal of Comparative Neurology · doi:10.1002/cne.901170206 · Cited by 79 · see citing works
Neocortical layers I and II of the hedgehog (Erinaceus europaeus)
Valverde, F., & Facal‐valverde, M. V. (1986) · Anatomy and Embryology · doi:10.1007/bf00318926 · Cited by 78 · see citing works
O’Rahilly, R., Müller, F., Hutchins, G. M., & Moore, G. W. (1987) · American Journal of Anatomy · doi:10.1002/aja.1001800106 · Cited by 76 · see citing works
The development of dendritic spines in the human visual cortex.
Ae, M., & Lj, G. (1984) · PubMed · Cited by 71 · see citing works
Gadisseux, J., Evrard, P., Misson, J., & Caviness, V. S. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90126-0 · Cited by 70 · see citing works
The marginal layer in the neocortex of a 7 week-old human embryo
Larroche, J. (1981) · Anatomy and Embryology · doi:10.1007/bf00299974 · Cited by 70 · see citing works
The development of the Xenopus retinofugal pathway: optic fibers join a pre-existing tract
Easter, S. S., & Taylor, J. S. H. (1989) · Development · doi:10.1242/dev.107.3.553 · Cited by 68 · see citing works
On the Early Development of the Isocortex in Fetal Sheep
Åarströum, K.-E. (1967) · Progress in brain research · doi:10.1016/s0079-6123(08)61418-1 · Cited by 67 · see citing works
Neurogenesis of the climbing fibers in the human cerebellum: A Golgi study
Marín‐Padilla, M. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902350107 · Cited by 61 · see citing works
Self-citationThe Organization of the Cerebral Cortex
Kernohan, J. W. (1957) · American Journal of Clinical Pathology · doi:10.1093/ajcp/28.1.88a · Cited by 59 · see citing works
M�ller, F., & O’Rahilly, R. (1988) · Anatomy and Embryology · doi:10.1007/bf00305100 · Cited by 48 · see citing works
The human brain at stage 16, including the initial evagination of the neurohypophysis
M�ller, F., & O’Rahilly, R. (1989) · Anatomy and Embryology · doi:10.1007/bf00315698 · Cited by 42 · see citing works
Comparative and Evolutionary Anatomy of the Visual Cortex of the Dolphin
Morgane, P. J., Glezer, I. I., & Jacobs, M. S. (1990) · Cerebral Cortex · doi:10.1007/978-1-4615-3824-0_4 · Cited by 41 · see citing works
Morphology of neurons in area 4γ of the cat's cortex studied with intracellular injection of HRP
Ghosh, S., Fyffe, R. E. W., & Porter, R. W. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902690212 · Cited by 39 · see citing works
Embryonic Vascularization of the Mammalian Cerebral Cortex
Marín‐Padilla, M. (1988) · Cerebral cortex · doi:10.1007/978-1-4615-6619-9_13 · Cited by 38 · see citing works
Self-citationDistribution of the apical dendritic spines of the layer V pyramidal cells of the hamster neocortex
Marín‐Padilla, M., & Stibitz, G. R. (1968) · Brain Research · doi:10.1016/0006-8993(68)90147-9 · Cited by 37 · see citing works
Self-citationClark University, 1889-1899: Decennial Celebration
Wilson, L. N., & Story, W. E. (2010) · Cited by 29 · see citing works
Powell, T. P. S., & Hendrickson, A. E. (1981) · Brain Research · doi:10.1016/0006-8993(81)90142-6 · Cited by 29 · see citing works
Marín‐Padilla, M. (1990) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1990.2.3.180 · Cited by 27 · see citing works
Self-citationSpine distribution of the layer V pyramidal cell in man: a cortical model
Marin-Padilla, M., Stibitz, G. R., Almy, C. P., & Brown, H. N. (1969) · Brain Research · doi:10.1016/0006-8993(69)90022-5 · Cited by 24 · see citing works
Modulatory Events in the Development and Evolution of Primate Neocortex
Jones, E. G. (1990) · Cerebral cortex · doi:10.1007/978-1-4757-9622-3_9 · Cited by 15 · see citing works
GROWTH AND PLASTICITY OF CORTICAL DENDRITES
Uylings, H. B. M., & Parnavelas, J. G. (1981) · Elsevier eBooks · doi:10.1016/b978-0-08-027372-3.50010-1 · Cited by 14 · see citing works
Clustering of dendrites in the cerebral cortex begins in the embryonic cortical plate
Hirst, E., Asante, J., & Price, J. (1991) · Journal of Neurocytology · doi:10.1007/bf01355539 · Cited by 12 · see citing works
Central Nervous System: Structure versus Injury and Regeneration versus Recovery
Marín‐Padilla, M. (1992) · Contemporary perspectives in neurosurgery · doi:10.1007/978-1-4612-2798-4_2 · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
1 of the 85 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Neuronal subtype specification in the cerebral cortex
Molyneaux, B. J., Arlotta, P., Menezes, J. R. L., & Macklis, J. D. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2151 · Cited by 1,632 · see citing works
Development and Evolution of the Human Neocortex
Lui, J. H., Hansen, D. V., & Kriegstein, A. R. (2011) · Cell · doi:10.1016/j.cell.2011.06.030 · Cited by 1,342 · see citing works
Glutamate Transporter Protein Subtypes Are Expressed Differentially during Rat CNS Development
Furuta, A., Rothstein, J. D., & Martin, L. J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08363.1997 · Cited by 552 · see citing works
Betizeau, M., Cortay, V., Patti, D., Pfister, S., Gautier, E., Bellemin-Ménard, A., Afanassieff, M., Huissoud, C., Douglas, R. J., Kennedy, H., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.032 · Cited by 462 · see citing works
Cajal–Retzius cells and the development of the neocortex
Marín‐Padilla, M. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01164-8 · Cited by 444 · see citing works
Self-citationZeng, H., Shen, E. H., Hohmann, J. G., Oh, S. W., Bernard, A., Royall, J. J., Glattfelder, K. J., Sunkin, S. M., Morris, J. A., Guillozet-Bongaarts, A. L., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.052 · Cited by 426 · see citing works
Diffusion tensor imaging of brain development
Hüppi, P. S., & Dubois, J. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.006 · Cited by 406 · see citing works
Diffusion tensor imaging of normal and injured developing human brain-a technical review
Neil, J., Miller, J., Mukherjee, P., & Hüppi, P. S. (2002) · NMR in Biomedicine · doi:10.1002/nbm.784 · Cited by 402 · see citing works
Bridging the Gap between Connectome and Transcriptome
Fornito, A., Arnatkevičiūtė, A., & Fulcher, B. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.10.005 · Cited by 380 · see citing works
Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway
Niu, S., Renfro, A., Quattrocchi, C. C., Sheldon, M., & D'Arcangelo, G. (2004) · Neuron · doi:10.1016/s0896-6273(03)00819-5 · Cited by 375 · see citing works
McKinstry, R. C. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.12.1237 · Cited by 373 · see citing works
Dysmaturation of Premature Brain: Importance, Cellular Mechanisms, and Potential Interventions
Volpe, J. J. (2019) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2019.02.016 · Cited by 365 · see citing works
Development of cortical microstructure in the preterm human brain
Ball, G., Srinivasan, L., Aljabar, P., Counsell, S. J., Durighel, G., Hajnal, J. V., Rutherford, M. A., & Edwards, A. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301652110 · Cited by 331 · see citing works
Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex
Hilgetag, C. C., & Barbas, H. (2006) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0020022 · Cited by 310 · see citing works
Cubelos, B., Sebastián‐Serrano, Á., Beccari, L. L., Calcagnotto, M. E., Cisneros, E., Kim, S., Dopazo, A., Álvarez‐Dolado, M., Redondo, J. M., Bovolenta, P., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.038 · Cited by 301 · see citing works
SOX5 Controls the Sequential Generation of Distinct Corticofugal Neuron Subtypes
Lai, T. S., Jabaudon, D., Molyneaux, B. J., Azim, E., Arlotta, P., Menezes, J. R. L., & Macklis, J. D. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.023 · Cited by 300 · see citing works
Tyzio, R., Represa, A., Jorquera, I., Ben-Ari, Y., Gozlan, H., & Aniksztejn, L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10372.1999 · Cited by 297 · see citing works
Demyanenko, G. P., Tsai, A. Y., & Maness, P. F. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-12-04907.1999 · Cited by 286 · see citing works
Nieuwenhuys, R. (1994) · Anatomy and Embryology · doi:10.1007/bf00187291 · Cited by 274 · see citing works
Molecular Control of Cortical Dendrite Development
Whitford, K. L., Dijkhuizen, P. A., Polleux, F., & Ghosh, A. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142932 · Cited by 266 · see citing works
Defining the Neurologic Consequences of Preterm Birth
Inder, T. E., Volpe, J. J., & Anderson, P. J. (2023) · New England Journal of Medicine · doi:10.1056/nejmra2303347 · Cited by 266 · see citing works
Delineation of early brain development from fetuses to infants with diffusion MRI and beyond
Ouyang, M., Dubois, J., Yu, Q., Mukherjee, P., & Huang, H. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.04.017 · Cited by 250 · see citing works
Invasive Procedures in Preterm Children: Brain and Cognitive Development at School Age
Vinall, J., Miller, S. P., Björnson, B., Fitzpatrick, K. P. V., Poskitt, K. J., Brant, R., Synnes, A. R., Cepeda, I. L., & GRUNAU, R. E. (2014) · PEDIATRICS · doi:10.1542/peds.2013-1863 · Cited by 256 · see citing works
Neural histology and neurogenesis of the human fetal and infant brain
Kostović, I., Sedmak, G., & Judáš, M. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.12.043 · Cited by 259 · see citing works
Neurite imaging reveals microstructural variations in human cerebral cortical gray matter
Fukutomi, H., Glasser, M. F., Zhang, H., Autio, J. A., Coalson, T. S., Okada, T., Togashi, K., Van Essen, D. C., & Hayashi, T. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.02.017 · Cited by 234 · see citing works
Diffusion Tensor Imaging and Tractography of Human Brain Development
Mukherjee, P., & McKinstry, R. C. (2006) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2005.11.004 · Cited by 223 · see citing works
The functions of the preplate in development and evolution of the neocortex and hippocampus
Supèr, H., Soriano, E., & Uylings, H. B. M. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00005-8 · Cited by 221 · see citing works
Dominguez, M. H., Ayoub, A. E., & RAKIC, P. T. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs252 · Cited by 209 · see citing works
Molecular insights into human brain evolution
Hill, R. S., & Walsh, C. A. (2005) · Nature · doi:10.1038/nature04103 · Cited by 208 · see citing works
Novel Subtype-Specific Genes Identify Distinct Subpopulations of Callosal Projection Neurons
Molyneaux, B. J., Arlotta, P., Fame, R. M., MacDonald, J. L., MacQuarrie, K. L., & Macklis, J. D. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6108-08.2009 · Cited by 198 · see citing works
Developmental mechanics of the primate cerebral cortex
Hilgetag, C. C., & Barbas, H. (2005) · Anatomy and Embryology · doi:10.1007/s00429-005-0041-5 · Cited by 198 · see citing works
Slower Postnatal Growth Is Associated with Delayed Cerebral Cortical Maturation in Preterm Newborns
Vinall, J., GRUNAU, R. E., Brant, R., Chau, V., Poskitt, K. J., Synnes, A. R., & Miller, S. P. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3004666 · Cited by 195 · see citing works
Biological effects after prenatal irradiation (embryo and fetus)
Valentin, J. (2003) · Annals of the ICRP · doi:10.1016/s0146-6453(03)00021-6 · Cited by 193 · see citing works
Krienen, F. M., Yeo, B. T. T., Ge, T., Buckner, R. L., & Sherwood, C. C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1510903113 · Cited by 190 · see citing works
Development of the Human Cortex and the Concept of “Critical” or “Sensitive” Periods
Uylings, H. B. M. (2006) · Language Learning · doi:10.1111/j.1467-9922.2006.00355.x · Cited by 189 · see citing works
Four Unique Interneuron Populations Reside in Neocortical Layer 1
Schuman, B., Machold, R. P., Hashikawa, Y., Fuzik, J., Fishell, G. J., & Rudy, B. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.1613-18.2018 · Cited by 184 · see citing works
“A later study from this group (Chu et al., 2003) showed that LS L1 INs had NGFC morphology. mystery” (Hubel, 1982; Marín-Padilla, 1992; Zhou and Hablitz, 1996a; Gilbert and Sigman, 2007; Palmer et al., 2012).”
BackgroundDevelopmental mechanisms underlying the evolution of human cortical circuits
Vanderhaeghen, P., & Polleux, F. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00675-z · Cited by 173 · see citing works
Vulnerability of cortical neurons to Alzheimer's and Parkinson's diseases
Braak, H., Rüb, U., Schultz, C., & Tredici, K. D. (2006) · Journal of Alzheimer s Disease · doi:10.3233/jad-2006-9s305 · Cited by 164 · see citing works
Diffusion tensor imaging of normal brain development
Yoshida, S., Oishi, K., Faria, A., & Mori, S. (2013) · Pediatric Radiology · doi:10.1007/s00247-012-2496-x · Cited by 145 · see citing works
McNab, J. A., Polimeni, J. R., Wang, R., Augustinack, J. C., Fujimoto, K., Stevens, A. A., Janssens, T., Farivar, R., Folkerth, R. D., Vanduffel, W., et al. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.11.065 · Cited by 158 · see citing works
The role of BAF (mSWI/SNF) complexes in mammalian neural development
Son, E., & Crabtree, G. R. (2014) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31416 · Cited by 151 · see citing works
Braak, H., & Del Tredici, K. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy152 · Cited by 148 · see citing works
Gautam, P., Anstey, K. J., Wen, W. X., Sachdev, P. S., & Cherbuin, N. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.03.018 · Cited by 141 · see citing works
The human brain intracerebral microvascular system: development and structure
Marín‐Padilla, M. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00038 · Cited by 140 · see citing works
Self-citationThe neurotransmitters and postsynaptic actions of callosally projecting neurons
Conti, F., & Manzoni, T. (1994) · Behavioural Brain Research · doi:10.1016/0166-4328(94)90117-1 · Cited by 143 · see citing works
Hutsler, J. J., Lee, D. G., & Porter, K. K. (2005) · Brain Research · doi:10.1016/j.brainres.2005.06.015 · Cited by 137 · see citing works
Marín‐Padilla, M. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903570407 · Cited by 136 · see citing works
Self-citationAboitiz, F., Morales, D., & Montiel, J. F. (2003) · Behavioral and Brain Sciences · doi:10.1017/s0140525x03000128 · Cited by 135 · see citing works
Morphological study of neocortical areas in Rett syndrome
Belichenko, P. V., Hagberg, B. A., & Dahlström, A. B. (1997) · Acta Neuropathologica · doi:10.1007/s004010050582 · Cited by 130 · see citing works
Boissart, C., Poulet, A., Georges, P., Darville, H., Julita, E., Delorme, R., Bourgeron, T., Peschanski, M., & Benchoua, A. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.71 · Cited by 128 · see citing works
Vidair, C. A. (2004) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2003.12.016 · Cited by 122 · see citing works
Morphological Development of Thick-Tufted Layer V Pyramidal Cells in the Rat Somatosensory Cortex
Romand, S., Wang, Y., Toledo-Rodriguez, M., & Markram, H. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00005 · Cited by 122 · see citing works
Interlaminar astroglia of the cerebral cortex: a marker of the primate brain
Colombo, J. A., & Reisin, H. D. (2004) · Brain Research · doi:10.1016/j.brainres.2004.02.003 · Cited by 132 · see citing works
Vasung, L., Lepage, C., Radoš, M., Pletikos, M., Goldman, J. S., Richiardi, J., Raguž, M., Fischi-Gómez, E., Karama, S., Hüppi, P. S., et al. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00011 · Cited by 121 · see citing works
Mallard, C. E., Rehn, A., Rees, S. M., Tolcos, M., & Copolov, D. (1999) · Schizophrenia Research · doi:10.1016/s0920-9964(99)00041-9 · Cited by 120 · see citing works
Kasper, E. M., Larkman, A. U., Lübke, J. H. R., & Blakemore, C. B. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903390403 · Cited by 119 · see citing works
Hutsler, J. J. (2003) · Brain and Language · doi:10.1016/s0093-934x(02)00531-x · Cited by 117 · see citing works
Sizonenko, S., Camm, E., Garbow, J., Maier, S., Inder, T., Williams, C., Neil, J., & Hüppi, P. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl168 · Cited by 110 · see citing works
Probing human brain evolution and development in organoids
Giandomenico, S. L., & Lancaster, M. A. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.01.001 · Cited by 107 · see citing works
The Cerebral Cortex Overlying Periventricular Leukomalacia: Analysis of Pyramidal Neurons
Andiman, S. E., Haynes, R. L., Trachtenberg, F. L., Billiards, S. S., Folkerth, R. D., Volpe, J. J., & Kinney, H. C. (2010) · Brain Pathology · doi:10.1111/j.1750-3639.2010.00380.x · Cited by 104 · see citing works
Moore, A. R., Filipovic, R., Mo, Z., Rasband, M. N., Zečević, N., & Antic, S. D. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn206 · Cited by 101 · see citing works
Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans
Caminiti, R., Innocenti, G. M., & Battaglia‐Mayer, A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.06.014 · Cited by 95 · see citing works
Nie, F., & Wong‐Riley, M. T. T. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990215)404:3 · Cited by 27 · see citing works
Rehn, A., van den Buuse, M., Copolov, D., Briscoe, T. A., Lambert, G. W., & Rees, S. M. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.07.047 · Cited by 95 · see citing works
Kasper, E. M., Lübke, J. H. R., Larkman, A. U., & Blakemore, C. B. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903390404 · Cited by 95 · see citing works
Fetal pain: implications for research and practice
Glover, V. A. S., & Fisk, N. M. (1999) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1999.tb08424.x · Cited by 95 · see citing works
Shaken infant syndrome: developmental neuropathology, progressive cortical dysplasia, and epilepsy
Marín‐Padilla, M., Parisi, J. E., Armstrong, D. L., Sargent, S., & Kaplan, J. A. (2002) · Acta Neuropathologica · doi:10.1007/s00401-001-0470-z · Cited by 94 · see citing works
Self-citationNeuroimaging of the Preterm Brain: Review and Recommendations
Inder, T. E., de Vries, L. S., Ferriero, D. M., Grant, P. E., Ment, L. R., Miller, S. P., & Volpe, J. J. (2021) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2021.06.014 · Cited by 90 · see citing works
Understanding the parietal lobe syndrome from a neurophysiological and evolutionary perspective
Caminiti, R., Chafee, M. V., Battaglia‐Mayer, A., Averbeck, B. B., Crowe, D. A., & Georgopoulos, A. P. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07291.x · Cited by 90 · see citing works
Galuske, R. A. W., & Singer, W. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.3.417 · Cited by 90 · see citing works
Romanski, L. M., Giguere, M., Bates, J. F., & Goldman-Rakic, P. S. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970317)379:3 · Cited by 325 · see citing works
Batalle, D., O'Muircheartaigh, J., Makropoulos, A., Kelly, C. J., Dimitrova, R., Hughes, E. J., Hajnal, J. V., Zhang, H., Alexander, D. C., Edwards, A. D., et al. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.05.046 · Cited by 89 · see citing works
Regional Dendritic Variation in Neonatal Human Cortex: A Quantitative Golgi Study
Travis, K., Ford, K., & Jacobs, B. (2005) · Developmental Neuroscience · doi:10.1159/000086707 · Cited by 89 · see citing works
Luque, J. M., Morante, J., & Fairén, A. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00604-1 · Cited by 85 · see citing works
Unc5C and DCC act downstream of Ctip2 and Satb2 and contribute to corpus callosum formation
Srivatsa, S., Parthasarathy, S., Britanova, O. V., Bormuth, I., Donahoo, A.-L. S., Ackerman, S. L., Richards, L. J., & Tarabykin, V. S. (2014) · Nature Communications · doi:10.1038/ncomms4708 · Cited by 84 · see citing works
Walkley, S. U. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.1028 · Cited by 84 · see citing works
Nomura, T., Takahashi, M., Hara, Y., & Osumi, N. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001454 · Cited by 84 · see citing works
de Lima, A. D., Merten, M. D. P., & Voigt, T. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970602)382:2 · Cited by 80 · see citing works
Multimodal Single-Cell Analysis Reveals Physiological Maturation in the Developing Human Neocortex
Mayer, S., Chen, J., Velmeshev, D., Mayer, A., Eze, U. C., Bhaduri, A., da Cunha, C. E., Jung, D., Arjun, A., Li, E., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.027 · Cited by 81 · see citing works
Wisco, J. J., Kuperberg, G. R., Manoach, D. S., Quinn, B. T., Busa, E., Fischl, B. R., Heckers, S., & Sorensen, A. G. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.03.031 · Cited by 80 · see citing works
Morphological properties of intracellularly labeled layer I neurons in rat neocortex
Zhou, F.-M., & Hablitz, J. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961209)376:2 · Cited by 79 · see citing works
The Early Differentiation of the Neocortex: a Hypothesis on Neocortical Evolution
Supèr, H. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.12.1101 · Cited by 73 · see citing works
Takahashi, E., Dai, G., Rosen, G., Wang, R.-P., Ohki, K., Folkerth, R., Galaburda, A., Wedeen, V., & Grant, P. E. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq084 · Cited by 70 · see citing works
Postlesional Epilepsy: The Ultimate Brain Plasticity
Jacobs, K. M., Graber, K., Kharazia, V., Parada, I., & Prince, D. A. (2000) · Epilepsia · doi:10.1111/j.1528-1157.2000.tb01574.x · Cited by 68 · see citing works
Herrick, T. M., & Cooper, J. A. (2002) · Development · doi:10.1242/dev.129.3.787 · Cited by 67 · see citing works
Earnest, D. J., Liang, F.-Q., DiGiorgio, S., Gallagher, M., Harvey, B. K., Earnest, B. J., & Seigel, G. M. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199904)39:1 · Cited by 49 · see citing works
Postnatal development of interhemispheric asymmetry in the cytoarchitecture of human area 4
Amunts, K., Schmidt-Passos, F., Schleicher, A., & Zilles, K. (1997) · Anatomy and Embryology · doi:10.1007/s004290050107 · Cited by 67 · see citing works
Neuronal Proliferation, Migration, Organization, and Myelination
Volpe, J. J. (2008) · Elsevier eBooks · doi:10.1016/b978-1-4160-3995-2.10002-0 · Cited by 65 · see citing works
Is the Late Preterm Infant More Vulnerable to Gray Matter Injury than the Term Infant?
Billiards, S. S., Pierson, C. R., Haynes, R. L., Folkerth, R. D., & Kinney, H. C. (2006) · Clinics in Perinatology · doi:10.1016/j.clp.2006.10.003 · Cited by 64 · see citing works
Yan, Y., van Brederode, J. F. M., & Hendrickson, A. E. (1995) · Journal of Neurocytology · doi:10.1007/bf01179982 · Cited by 62 · see citing works
Localisation of amino acid neurotransmitters during postnatal development of the rat retina
Fletcher, E. L., & Kalloniatis, M. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970421)380:4 · Cited by 99 · see citing works
Verney, C., & Derer, P. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903590110 · Cited by 58 · see citing works
Ouyang, M., Liu, P., Jeon, T., Chalak, L. F., Heyne, R. J., Rollins, N. K., Licht, D. J., Detre, J. A., Roberts, T. P. L., Lu, H., et al. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.12.034 · Cited by 57 · see citing works
Popken, G. J., & Farel, P. B. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970915)386:1 · Cited by 117 · see citing works
Expression of neuronal nitric oxide synthase during embryonic development of the rat cerebral cortex
Santacana, M., UTTENTHAL, L. O., Bentura, M. L., Fernández, A. P., Serrano, J., de Velasco, J. M., Alonso, D. C., Martínez‐Murillo, R., & Rodrigo, J. (1998) · Developmental Brain Research · doi:10.1016/s0165-3806(98)00140-0 · Cited by 54 · see citing works
Transient increase of tenascin-C in immature hippocampus: astroglial and neuronal expression
Ferhat, L., Chevassus-au-Louis, N., Jorquera, I., Niquet, J., Khrestchatisky, M., Ben‐Ari, Y., & Represa, A. (1996) · Journal of Neurocytology · doi:10.1007/bf02284785 · Cited by 52 · see citing works
Ha, S., & Redmond, L. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20682 · Cited by 51 · see citing works
Stepien, B. K., Vaid, S., & Huttner, W. Β. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.676911 · Cited by 50 · see citing works
Regulation of dendritic growth by calcium and neurotrophin signaling
Dijkhuizen, P. A., & Ghosh, A. (2004) · Progress in brain research · doi:10.1016/s0079-6123(04)47002-2 · Cited by 50 · see citing works
The existence of a layer IV in the rat motor cortex
Skoglund, T. S. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.2.178 · Cited by 50 · see citing works
- Authors
- Marín‐Padilla, M.
- Affiliations
- Dartmouth College (US)
- Corresponding author
- Marín‐Padilla, Miguel
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1992-07-08
- Volume
- 321
- Issue
- 2
- Pages
- 223-240
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2098862557
- Cited by
- 285
- References
- 85
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 9 · 2023: 10 · 2022: 1 · 2021: 13 · 2020: 10 · 2019: 9 · 2018: 11 · 2017: 6 · 2016: 9 · 2015: 7 · 2014: 9 · 2013: 11 · 2012: 9
- FWCI
- 5.11
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ns022897-10)
- National Institute of Neurological Disorders and Stroke (NS22897)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- neocortex development, pyramidal neurons, cortical plate, neuronal migration, radial glial fibers, apical dendrites, cortical maturation, layer I, mammalian evolution, cortical expansion, comparative neuroanatomy
- MeSH terms
- Animals, Cats, Cell Differentiation, Cerebral Cortex, Biological Evolution, Female, Embryonic and Fetal Development, Fetus, Cricetinae, Histocytochemistry, Humans, Neurons, Phenotype, Pregnancy, Pyramidal Tracts, Species Specificity, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
