Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 8 July 1988:
Vol. 241. no. 4862, pp. 170 - 176
DOI: 10.1126/science.3291116

Articles

Science, Vol 241, Issue 4862, 170-176
Copyright © 1988 by American Association for the Advancement of Science


articles

Specification of cerebral cortical areas

P Rakic

Yale University School of Medicine, New Haven, CT 06510.

How the immense population of neurons that constitute the human cerebral neocortex is generated from progenitors lining the cerebral ventricle and then distributed to appropriate layers of distinctive cytoarchitectonic areas can be explained by the radial unit hypothesis. According to this hypothesis, the ependymal layer of the embryonic cerebral ventricle consists of proliferative units that provide a proto-map of prospective cytoarchitectonic areas. The output of the proliferative units is translated via glial guides to the expanding cortex in the form of ontogenetic columns, whose final number for each area can be modified through interaction with afferent input. Data obtained through various advanced neurobiological techniques, including electron microscopy, immunocytochemistry, [3H]thymidine and receptor autoradiography, retrovirus gene transfer, neural transplants, and surgical or genetic manipulation of cortical development, furnish new details about the kinetics of cell proliferation, their lineage relationships, and phenotypic expression that favor this hypothesis. The radial unit model provides a framework for understanding cerebral evolution, epigenetic regulation of the parcellation of cytoarchitectonic areas, and insight into the pathogenesis of certain cortical disorders in humans.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Selective Cortical Layering Abnormalities and Behavioral Deficits in Cortex-Specific Pax6 Knock-Out Mice.
T. C. Tuoc, K. Radyushkin, A. B. Tonchev, M. C. Pinon, R. Ashery-Padan, Z. Molnar, M. S. Davidoff, and A. Stoykova (2009)
J. Neurosci. 29, 8335-8349
   Abstract »    Full Text »    PDF »
Origin, Early Commitment, Migratory Routes, and Destination of Cannabinoid Type 1 Receptor-Containing Interneurons.
Y. M. Morozov, M. Torii, and P. Rakic (2009)
Cereb Cortex 19, i78-i89
   Abstract »    Full Text »    PDF »
Spatial Distribution of Deep Sulcal Landmarks and Hemispherical Asymmetry on the Cortical Surface.
K. Im, H. J. Jo, J.-F. Mangin, A. C. Evans, S. I. Kim, and J.-M. Lee (2009)
Cereb Cortex
   Abstract »    Full Text »    PDF »
Effects of Bilateral Enucleation on the Size of Visual and Nonvisual Areas of the Brain.
S. J. Karlen and L. Krubitzer (2009)
Cereb Cortex 19, 1360-1371
   Abstract »    Full Text »    PDF »
Brca1 is required for embryonic development of the mouse cerebral cortex to normal size by preventing apoptosis of early neural progenitors.
J. N. Pulvers and W. B. Huttner (2009)
Development 136, 1859-1868
   Abstract »    Full Text »    PDF »
Anterior cingulate cortex abnormalities associated with a first psychotic episode in bipolar disorder.
A. Fornito, M. Yucel, S. J. Wood, A. Bechdolf, S. Carter, C. Adamson, D. Velakoulis, M. M. Saling, P. D. McGorry, and C. Pantelis (2009)
The British Journal of Psychiatry 194, 426-433
   Abstract »    Full Text »    PDF »
Anatomical Characterization of Human Fetal Brain Development with Diffusion Tensor Magnetic Resonance Imaging.
H. Huang, R. Xue, J. Zhang, T. Ren, L. J. Richards, P. Yarowsky, M. I. Miller, and S. Mori (2009)
J. Neurosci. 29, 4263-4273
   Abstract »    Full Text »    PDF »
Differential Regulation of Telencephalic Pallial-Subpallial Boundary Patterning by Pax6 and Gsh2.
R. S.E. Carney, L. A. Cocas, T. Hirata, K. Mansfield, and J. G. Corbin (2009)
Cereb Cortex 19, 745-759
   Abstract »    Full Text »    PDF »
Distinct Genetic Influences on Cortical Surface Area and Cortical Thickness.
M. S. Panizzon, C. Fennema-Notestine, L. T. Eyler, T. L. Jernigan, E. Prom-Wormley, M. Neale, K. Jacobson, M. J. Lyons, M. D. Grant, C. E. Franz, et al. (2009)
Cereb Cortex
   Abstract »    Full Text »    PDF »
Thick Visual Cortex in the Early Blind.
J. Jiang, W. Zhu, F. Shi, Y. Liu, J. Li, W. Qin, K. Li, C. Yu, and T. Jiang (2009)
J. Neurosci. 29, 2205-2211
   Abstract »    Full Text »    PDF »
Layer-Specific Expression of Multiple Cadherins in the Developing Visual Cortex (V1) of the Ferret.
Krishna-K, M. Nuernberger, F. Weth, and C. Redies (2009)
Cereb Cortex 19, 388-401
   Abstract »    Full Text »    PDF »
Intermediate Neuronal Progenitors (Basal Progenitors) Produce Pyramidal-Projection Neurons for All Layers of Cerebral Cortex.
T. Kowalczyk, A. Pontious, C. Englund, R. A. M. Daza, F. Bedogni, R. Hodge, A. Attardo, C. Bell, W. B. Huttner, and R. F. Hevner (2009)
Cereb Cortex
   Abstract »    Full Text »    PDF »
Alterations in Midline Cortical Thickness and Gyrification Patterns Mapped in Children with 22q11.2 Deletions.
C. E. Bearden, T. G.M. van Erp, R. A. Dutton, A. D. Lee, T. J. Simon, T. D. Cannon, B. S. Emanuel, D. McDonald-McGinn, E. H. Zackai, and P. M. Thompson (2009)
Cereb Cortex 19, 115-126
   Abstract »    Full Text »    PDF »
HP1-{beta} is required for development of the cerebral neocortex and neuromuscular junctions.
R. Aucott, J. Bullwinkel, Y. Yu, W. Shi, M. Billur, J. P. Brown, U. Menzel, D. Kioussis, G. Wang, I. Reisert, et al. (2008)
J. Cell Biol. 183, 597-606
   Abstract »    Full Text »    PDF »
Small focal cortical dysplasia lesions are located at the bottom of a deep sulcus.
P. Besson, F. Andermann, F. Dubeau, and A. Bernasconi (2008)
Brain 131, 3246-3255
   Abstract »    Full Text »    PDF »
Modes and Mishaps of Neuronal Migration in the Mammalian Brain.
C. Metin, R. B. Vallee, P. Rakic, and P. G. Bhide (2008)
J. Neurosci. 28, 11746-11752
   Abstract »    Full Text »    PDF »
Temporal control of neuronal diversity: common regulatory principles in insects and vertebrates?.
J. Jacob, C. Maurange, and A. P. Gould (2008)
Development 135, 3481-3489
   Abstract »    Full Text »    PDF »
Radial Glia Cells in the Developing Human Brain.
B. M. Howard, Zhicheng Mo, R. Filipovic, A. R. Moore, S. D. Antic, and N. Zecevic (2008)
Neuroscientist 14, 459-473
   Abstract »    PDF »
Gene Expression in Cortical Interneuron Precursors is Prescient of their Mature Function.
R. Batista-Brito, R. Machold, C. Klein, and G. Fishell (2008)
Cereb Cortex 18, 2306-2317
   Abstract »    Full Text »    PDF »
Brain Size and Folding of the Human Cerebral Cortex.
R. Toro, M. Perron, B. Pike, L. Richer, S. Veillette, Z. Pausova, and T. Paus (2008)
Cereb Cortex 18, 2352-2357
   Abstract »    Full Text »    PDF »
Expression of liver X receptor {beta} is essential for formation of superficial cortical layers and migration of later-born neurons.
X. Fan, H.-J. Kim, D. Bouton, M. Warner, and J.-A. Gustafsson (2008)
PNAS 105, 13445-13450
   Abstract »    Full Text »    PDF »
Making bigger brains-the evolution of neural-progenitor-cell division.
J. L. Fish, C. Dehay, H. Kennedy, and W. B. Huttner (2008)
J. Cell Sci. 121, 2783-2793
   Abstract »    Full Text »    PDF »
Mapping the Relationship between Cortical Convolution and Intelligence: Effects of Gender.
E. Luders, K. L. Narr, R. M. Bilder, P. R. Szeszko, M. N. Gurbani, L. Hamilton, A. W. Toga, and C. Gaser (2008)
Cereb Cortex 18, 2019-2026
   Abstract »    Full Text »    PDF »
COUP-TFI Coordinates Cortical Patterning, Neurogenesis, and Laminar Fate and Modulates MAPK/ERK, AKT, and ss-Catenin Signaling.
A. Faedo, G. S. Tomassy, Y. Ruan, H. Teichmann, S. Krauss, S. J. Pleasure, S. Y. Tsai, M.-J. Tsai, M. Studer, and J. L. R. Rubenstein (2008)
Cereb Cortex 18, 2117-2131
   Abstract »    Full Text »    PDF »
Brain Size and Cortical Structure in the Adult Human Brain.
K. Im, J.-M. Lee, O. Lyttelton, S. H. Kim, A. C. Evans, and S. I. Kim (2008)
Cereb Cortex 18, 2181-2191
   Abstract »    Full Text »    PDF »
Altered Molecular Regionalization and Normal Thalamocortical Connections in Cortex-Specific Pax6 Knock-Out Mice.
M. C. Pinon, T. C. Tuoc, R. Ashery-Padan, Z. Molnar, and A. Stoykova (2008)
J. Neurosci. 28, 8724-8734
   Abstract »    Full Text »    PDF »
From the Cover: The basic nonuniformity of the cerebral cortex.
S. Herculano-Houzel, C. E. Collins, P. Wong, J. H. Kaas, and R. Lent (2008)
PNAS 105, 12593-12598
   Abstract »    Full Text »    PDF »
Confusing cortical columns.
P. Rakic (2008)
PNAS 105, 12099-12100
   Full Text »    PDF »
The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone.
X. Liu, K. Hashimoto-Torii, M. Torii, T. F. Haydar, and P. Rakic (2008)
PNAS 105, 11802-11807
   Abstract »    Full Text »    PDF »
Lis1-Nde1-dependent neuronal fate control determines cerebral cortical size and lamination.
A. S. Pawlisz, C. Mutch, A. Wynshaw-Boris, A. Chenn, C. A. Walsh, and Y. Feng (2008)
Hum. Mol. Genet. 17, 2441-2455
   Abstract »    Full Text »    PDF »
Cortical Folding Patterns and Predicting Cytoarchitecture.
B. Fischl, N. Rajendran, E. Busa, J. Augustinack, O. Hinds, B.T. T. Yeo, H. Mohlberg, K. Amunts, and K. Zilles (2008)
Cereb Cortex 18, 1973-1980
   Abstract »    Full Text »    PDF »
A Molecular Neuroanatomical Study of the Developing Human Neocortex from 8 to 17 Postconceptional Weeks Revealing the Early Differentiation of the Subplate and Subventricular Zone.
N. Bayatti, J. A. Moss, L. Sun, P. Ambrose, J. F. H. Ward, S. Lindsay, and G. J. Clowry (2008)
Cereb Cortex 18, 1536-1548
   Abstract »    Full Text »    PDF »
Early Telencephalic Migration Topographically Converging in the Olfactory Cortex.
F. Garcia-Moreno, L. Lopez-Mascaraque, and J. A. de Carlos (2008)
Cereb Cortex 18, 1239-1252
   Abstract »    Full Text »    PDF »
Deep Sulcal Landmarks Provide an Organizing Framework for Human Cortical Folding.
G. Lohmann, D. Y. von Cramon, and A. C. F. Colchester (2008)
Cereb Cortex 18, 1415-1420
   Abstract »    Full Text »    PDF »
Mapping the Early Cortical Folding Process in the Preterm Newborn Brain.
J Dubois, M Benders, A Cachia, F Lazeyras, R Ha-Vinh Leuchter, S. V. Sizonenko, C Borradori-Tolsa, J. F. Mangin, and P. S. Huppi (2008)
Cereb Cortex 18, 1444-1454
   Abstract »    Full Text »    PDF »
Basal temporal sulcal morphology in healthy controls and patients with temporal lobe epilepsy.
H. Kim, N. Bernasconi, B. Bernhardt, O. Colliot, and A. Bernasconi (2008)
Neurology 70, 2159-2165
   Abstract »    Full Text »    PDF »
Dynamic ATP signalling and neural development.
N. Dale (2008)
J. Physiol. 586, 2429-2436
   Abstract »    Full Text »    PDF »
Morphology of the Ventral Frontal Cortex: Relationship to Femininity and Social Cognition.
J. L. Wood, D. Heitmiller, N. C. Andreasen, and P. Nopoulos (2008)
Cereb Cortex 18, 534-540
   Abstract »    Full Text »    PDF »
Nuclear Receptor TLX Regulates Cell Cycle Progression in Neural Stem Cells of the Developing Brain.
W. Li, G. Sun, S. Yang, Q. Qu, K. Nakashima, and Y. Shi (2008)
Mol. Endocrinol. 22, 56-64
   Abstract »    Full Text »    PDF »
Orbitofrontal volume deficit in schizophrenia and thought disorder.
M. Nakamura, P. G. Nestor, J. J. Levitt, A. S. Cohen, T. Kawashima, M. E. Shenton, and R. W. McCarley (2008)
Brain 131, 180-195
   Abstract »    Full Text »    PDF »
Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex.
M. R. Costa, G. Wen, A. Lepier, T. Schroeder, and M. Gotz (2008)
Development 135, 11-22
   Abstract »    Full Text »    PDF »
Disruption of Neuronal Migration by RNAi of Dyx1c1 Results in Neocortical and Hippocampal Malformations.
G. D. Rosen, J. Bai, Y. Wang, C. G. Fiondella, S. W. Threlkeld, J. J. LoTurco, and A. M. Galaburda (2007)
Cereb Cortex 17, 2562-2572
   Abstract »    Full Text »    PDF »
Developmental Changes and Injury Induced Disruption of the Radial Organization of the Cortex in the Immature Rat Brain Revealed by In Vivo Diffusion Tensor MRI.
S. V. Sizonenko, E. J. Camm, J. R. Garbow, S. E. Maier, T. E. Inder, C. E. Williams, J. J. Neil, and P. S. Huppi (2007)
Cereb Cortex 17, 2609-2617
   Abstract »    Full Text »    PDF »
Computational Models of Neocortical Neuronogenesis and Programmed Cell Death in the Developing Mouse, Monkey, and Human.
J. M. Gohlke, W. C. Griffith, and E. M. Faustman (2007)
Cereb Cortex 17, 2433-2442
   Abstract »    Full Text »    PDF »
Reduced Neocortical Thickness and Complexity Mapped in Mesial Temporal Lobe Epilepsy with Hippocampal Sclerosis.
J. J. Lin, N. Salamon, A. D. Lee, R. A. Dutton, J. A. Geaga, K. M. Hayashi, E. Luders, A. W. Toga, J. Engel Jr, and P. M. Thompson (2007)
Cereb Cortex 17, 2007-2018
   Abstract »    Full Text »    PDF »
Genetic Analysis of Anterior Posterior Expression Gradients in the Developing Mammalian Forebrain.
L. C. Kudo, S. L. Karsten, J. Chen, P. Levitt, and D. H. Geschwind (2007)
Cereb Cortex 17, 2108-2122
   Abstract »    Full Text »    PDF »
Competing Interactions between Micro-RNAs Determine Neural Progenitor Survival and Proliferation after Ethanol Exposure: Evidence from an Ex Vivo Model of the Fetal Cerebral Cortical Neuroepithelium.
P. Sathyan, H. B. Golden, and R. C. Miranda (2007)
J. Neurosci. 27, 8546-8557
   Abstract »    Full Text »    PDF »
Handedness Is Associated with Asymmetries in Gyrification of the Cerebral Cortex of Chimpanzees.
W. D. Hopkins, C. Cantalupo, and J. Taglialatela (2007)
Cereb Cortex 17, 1750-1756
   Abstract »    Full Text »    PDF »
Comparative Analysis of Layer-Specific Genes in Mammalian Neocortex.
A. Watakabe, N. Ichinohe, S. Ohsawa, T. Hashikawa, Y. Komatsu, K. S. Rockland, and T. Yamamori (2007)
Cereb Cortex 17, 1918-1933
   Abstract »    Full Text »    PDF »
Novel IgCAM, MDGA1, Expressed in Unique Cortical Area- and Layer-Specific Patterns and Transiently by Distinct Forebrain Populations of Cajal-Retzius Neurons.
A. Takeuchi, T. Hamasaki, E. D. Litwack, and D. D.M. O'Leary (2007)
Cereb Cortex 17, 1531-1541
   Abstract »    Full Text »    PDF »
Oculomotor Control in Children Who Were Born Very Prematurely.
D. Newsham, P. C. Knox, and R. W. I. Cooke (2007)
Invest. Ophthalmol. Vis. Sci. 48, 2595-2601
   Abstract »    Full Text »    PDF »
Plasticity of the Primate Prefrontal Cortex.
S. Kuboshima-Amemori and T. Sawaguchi (2007)
Neuroscientist 13, 229-240
   Abstract »    PDF »
Patterning of frontal cortex subdivisions by Fgf17.
J. A. Cholfin and J. L. R. Rubenstein (2007)
PNAS 104, 7652-7657
   Abstract »    Full Text »    PDF »
Altered orbitofrontal sulcogyral pattern in schizophrenia.
M. Nakamura, P. G. Nestor, R. W. McCarley, J. J. Levitt, L. Hsu, T. Kawashima, M. Niznikiewicz, and M. E. Shenton (2007)
Brain 130, 693-707
   Abstract »    Full Text »    PDF »
Perinatal risk factors altering regional brain structure in the preterm infant.
D. K. Thompson, S. K. Warfield, J. B. Carlin, M. Pavlovic, H. X. Wang, M. Bear, M. J. Kean, L. W. Doyle, G. F. Egan, and T. E. Inder (2007)
Brain 130, 667-677
   Abstract »    Full Text »    PDF »
Cellular scaling rules for primate brains.
S. Herculano-Houzel, C. E. Collins, P. Wong, and J. H. Kaas (2007)
PNAS 104, 3562-3567
   Abstract »    Full Text »    PDF »
A Temporal Continuity to the Vertical Organization of the Human Neocortex.
M. F. Casanova, J. Trippe II, and A. Switala (2007)
Cereb Cortex 17, 130-137
   Abstract »    Full Text »    PDF »
Cell-Autonomous beta-Catenin Signaling Regulates Cortical Precursor Proliferation.
G. J. Woodhead, C. A. Mutch, E. C. Olson, and A. Chenn (2006)
J. Neurosci. 26, 12620-12630
   Abstract »    Full Text »    PDF »
Diffusion Tensor Imaging Reveals White Matter Reorganization in Early Blind Humans.
J.S. Shimony, H. Burton, A.A. Epstein, D.G. McLaren, S.W. Sun, and A.Z. Snyder (2006)
Cereb Cortex 16, 1653-1661
   Abstract »    Full Text »    PDF »
Spatial patterns of cortical thinning in mild cognitive impairment and Alzheimer's disease.
V. Singh, H. Chertkow, J. P. Lerch, A. C. Evans, A. E. Dorr, and N. J. Kabani (2006)
Brain 129, 2885-2893
   Abstract »    Full Text »    PDF »
From the Cover: Prenatal exposure to ultrasound waves impacts neuronal migration in mice.
E. S. B. C. Ang Jr, V. Gluncic, A. Duque, M. E. Schafer, and P. Rakic (2006)
PNAS 103, 12903-12910
   Abstract »    Full Text »    PDF »
Stable neuron numbers from cradle to grave.
R. S. Nowakowski (2006)
PNAS 103, 12219-12220
   Full Text »    PDF »
Dendritic Size of Pyramidal Neurons Differs among Mouse Cortical Regions.
R. Benavides-Piccione, F. Hamzei-Sichani, I. Ballesteros-Yanez, J. DeFelipe, and R. Yuste (2006)
Cereb Cortex 16, 990-1001
   Abstract »    Full Text »    PDF »
Activity-dependent Expression of occ1 in Excitatory Neurons Is a Characteristic Feature of the Primate Visual Cortex.
T. Takahata, Y. Komatsu, A. Watakabe, T. Hashikawa, S. Tochitani, and T. Yamamori (2006)
Cereb Cortex 16, 929-940
   Abstract »    Full Text »    PDF »
The postnatal development of neocortical neurons and glial cells in the Gottingen minipig and the domestic pig brain.
J. Jelsing, R. Nielsen, A. K. Olsen, N. Grand, R. Hemmingsen, and B. Pakkenberg (2006)
J. Exp. Biol. 209, 1454-1462
   Abstract »    Full Text »    PDF »
BDNF-modulated Spatial Organization of Cajal-Retzius and GABAergic Neurons in the Marginal Zone Plays a Role in the Development of Cortical Organization.
S. Alcantara, E. Pozas, C. F. Ibanez, and E. Soriano (2006)
Cereb Cortex 16, 487-499
   Abstract »    Full Text »    PDF »
Molecular and Morphological Heterogeneity of Neural Precursors in the Mouse Neocortical Proliferative Zones.
J. S. Gal, Y. M. Morozov, A. E. Ayoub, M. Chatterjee, P. Rakic, and T. F. Haydar (2006)
J. Neurosci. 26, 1045-1056
   Abstract »    Full Text »    PDF »
Role of the Protomap and Target-derived Signals in the Development of Intrahemispheric Connections.
W. Bai, M. Ishida, M. Okabe, and Y. Arimatsu (2006)
Cereb Cortex 16, 124-135
   Abstract »    Full Text »    PDF »
Neuronal Migration Disorders.
P. Gressens (2005)
J Child Neurol 20, 968-971
   Abstract »    PDF »
A Morphogenetic Model for the Development of Cortical Convolutions.
R. Toro and Y. Burnod (2005)
Cereb Cortex 15, 1900-1913
   Abstract »    Full Text »    PDF »
Patterning and Plasticity of the Cerebral Cortex.
M. Sur and J. L. R. Rubenstein (2005)
Science 310, 805-810
   Abstract »    Full Text »    PDF »
DPP signaling controls development of the lamina glia required for retinal axon targeting in the visual system of Drosophila.
S. Yoshida, L. Soustelle, A. Giangrande, D. Umetsu, S. Murakami, T. Yasugi, T. Awasaki, K. Ito, M. Sato, and T. Tabata (2005)
Development 132, 4587-4598
   Abstract »    Full Text »    PDF »
Genomic characterisation of a Fgf-regulated gradient-based neocortical protomap.
S. N. Sansom, J. M. Hebert, U. Thammongkol, J. Smith, G. Nisbet, M. A. Surani, S. K. McConnell, and F. J. Livesey (2005)
Development 132, 3947-3961
   Abstract »    Full Text »    PDF »
Genetic Contributions to Human Gyrification: Sulcal Morphometry in Williams Syndrome.
J. S. Kippenhan, R. K. Olsen, C. B. Mervis, C. A. Morris, P. Kohn, A. Meyer-Lindenberg, and K. F. Berman (2005)
J. Neurosci. 25, 7840-7846
   Abstract »    Full Text »    PDF »
Fibroblast Growth Factor 8 Regulates Neocortical Guidance of Area-Specific Thalamic Innervation.
T. Shimogori and E. A. Grove (2005)
J. Neurosci. 25, 6550-6560
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)