Neurons in Rhesus Monkey Visual Cortex: Systematic Relation between Time of Origin and Eventual Disposition
Abstract
Autoradiographic evidence after injection of tritiated thymidine indicates that cell position in the laminae of the monkey visual cortex is systematically related to time of cell origin. The earliest-formed neurons, destined for the deepest stratum, arise at about embryonic day 45, and the last ones, destined for the outermost cell stratum, form at about day 102; cells of intervening layers are generated at intervening times. No neocortical neurons are produced in the last two prenatal months or after birth. Compared to cortical neurons in rodents, those in the monkey arise earlier, and the "inside-out" relation of cell position to time of origin is more rigid.
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?
The generation of the six-layer cortical plate occurs in an inside-out fashion, with early-born neurons establishing layer 6, then layer 5, and so forth.
“The generation of the six-layer cortical plate occurs in an inside-out fashion, with the early-born neurons establishing layer 6, then layer 5, and so forth59.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [59]
Cites
Caviness, V. S., & Sidman, R. L. (1973) · Journal of Comparative Neurology · doi:10.1002/cne.901480202 · Cited by 413 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Specification of Cerebral Cortical Areas
Rakic, P. (1988) · Science · doi:10.1126/science.3291116 · Cited by 3,127 · see citing works
Self-citationNoctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229 · see citing works
Evolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565 · see citing works
Self-citationStructural and functional brain development and its relation to cognitive development
Casey, B. J., Giedd, J. N., & Thomas, K. M. (2000) · Biological Psychology · doi:10.1016/s0301-0511(00)00058-2 · Cited by 1,506 · 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
Neurogenic radial glia in the outer subventricular zone of human neocortex
Hansen, D. V., Lui, J. H., Parker, P. R. L., & Kriegstein, A. R. (2010) · Nature · doi:10.1038/nature08845 · Cited by 1,388 · 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
Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex
Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986) · Science · doi:10.1126/science.3952506 · Cited by 1,133 · see citing works
Self-citationRakic, P. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93934-p · Cited by 1,047 · see citing works
Self-citationSpatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex
Nowakowski, T. J., Bhaduri, A., Pollen, A. A., Alvarado, B., Mostajo-Radji, M. A., Di Lullo, E., Haeussler, M., Sandoval-Espinosa, C., Liu, S. J., Velmeshev, D., et al. (2017) · Science · doi:10.1126/science.aap8809 · Cited by 964 · see citing works
Kadoshima, T., Sakaguchi, H., Nakano, T., Soen, M., Ando, S., Eiraku, M., & Sasai, Y. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315710110 · Cited by 999 · see citing works
Microglia Regulate the Number of Neural Precursor Cells in the Developing Cerebral Cortex
Cunningham, C. L., Martínez-Cerdeño, V., & Noctor, S. C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3441-12.2013 · Cited by 976 · see citing works
Akbarian, S. (1995) · Archives of General Psychiatry · doi:10.1001/archpsyc.1995.03950160008002 · Cited by 1,002 · see citing works
Development of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977 · see citing works
Self-citationMolecular logic of neocortical projection neuron specification, development and diversity
Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H., & Macklis, J. D. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3586 · Cited by 863 · 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
Lavdas, A. A., Grigoriou, M., Pachnis, V., & Parnavelas, J. G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07881.1999 · Cited by 765 · see citing works
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687 · see citing works
Prenatal genesis of connections subserving ocular dominance in the rhesus monkey
Rakic, P. (1976) · Nature · doi:10.1038/261467a0 · Cited by 677 · see citing works
Self-citationRole of the Reelin Signaling Pathway in Central Nervous System Development
Rice, D. S., & Curran, T. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1005 · Cited by 667 · see citing works
Cell-cycle control and cortical development
Dehay, C., & Kennedy, H. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2097 · Cited by 655 · see citing works
Allendoerfer, K. L., & Shatz, C. J. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.001153 · Cited by 653 · see citing works
Taupin, P. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.08.002 · Cited by 645 · see citing works
Synaptic development of the cerebral cortex: implications for learning, memory and mental illness
(1994) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60543-9 · Cited by 565 · see citing works
Do cortical areas emerge from a protocortex?
O'Leary, D. D. M. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90080-5 · Cited by 536 · see citing works
A new subtype of progenitor cell in the mouse embryonic neocortex
Wang, X., Tsai, J.-W., LaMonica, B., & Kriegstein, A. R. (2011) · Nature Neuroscience · doi:10.1038/nn.2807 · Cited by 507 · 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
Induction of Expansion and Folding in Human Cerebral Organoids
Li, Y., Muffat, J., Omer, A., Bosch, I., Lancaster, M. A., Sur, M., Gehrke, L., Knoblich, J. A., & Jaenisch, R. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2016.11.017 · Cited by 436 · see citing works
Development and arealization of the cerebral cortex
Cadwell, C. R., Bhaduri, A., Mostajo-Radji, M. A., Keefe, M. G., & Nowakowski, T. J. (2019) · Neuron · doi:10.1016/j.neuron.2019.07.009 · Cited by 408 · see citing works
Neocortical neurogenesis in humans is restricted to development
Bhardwaj, R. D., Curtis, M. A., Spalding, K. L., Buchholz, B. A., Fink, D., Björk-Eriksson, T., Nordborg, C., Gage, F. H., Druid, H., Eriksson, P. S., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605177103 · Cited by 448 · see citing works
Guiding Neuronal Cell Migrations
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
Self‐organized developmental patterning and differentiation in cerebral organoids
Renner, M., Lancaster, M. A., Bian, S., Choi, H., Ku, T., Peer, A., Chung, K., & Knoblich, J. A. (2017) · The EMBO Journal · doi:10.15252/embj.201694700 · Cited by 389 · see citing works
Miyoshi, G., Butt, S. J. B., Takebayashi, H., & Fishell, G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1807-07.2007 · Cited by 400 · see citing works
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“C Illustration of the dynamics of major developmental events and diversity of progenitors involved in the development of primate cerebral neocortex based on studies of Rakic, with permission from Silver et al. [396].”
MethodInfluentialSelf-citationDevelopment, specification, and diversity of callosal projection neurons
Fame, R. M., MacDonald, J. L., & Macklis, J. D. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2010.10.002 · Cited by 381 · see citing works
New evidence for neurotransmitter influences on brain development
Levitt, P., Harvey, J. A., Friedman, E., Simansky, K., & Murphy, E. H. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01028-4 · Cited by 362 · see citing works
Schizophrenia: a tale of two critical periods for prefrontal cortical development
Selemon, L. D., & Zecevic, N. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.115 · Cited by 336 · see citing works
Characterization of Nkx6-2-Derived Neocortical Interneuron Lineages
Sousa, V. H., Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., & Fishell, G. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp038 · Cited by 328 · see citing works
G1 Phase Regulation, Area-Specific Cell Cycle Control, and Cytoarchitectonics in the Primate Cortex
Lukaszewicz, A., Savatier, P., Cortay, V., Giroud, P., Huissoud, C., Berland, M., Kennedy, H., & Dehay, C. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.032 · Cited by 315 · see citing works
Evolutionary changes in promoter and enhancer activity during human corticogenesis
Reilly, S. K., Yin, J., Ayoub, A. E., Emera, D., Leng, J., Cotney, J., Sarro, R., Rakic, P., & Noonan, J. P. (2015) · Science · doi:10.1126/science.1260943 · Cited by 297 · see citing works
Self-citationBauman, M. D., Iosif, A.-M., Smith, S. E. P., Bregere, C., Amaral, D. G., & Patterson, P. H. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.025 · Cited by 294 · see citing works
Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex
Ang, E. S. B. C., Haydar, T. F., Gluncic, V., & Rakic, P. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05805.2003 · Cited by 282 · see citing works
Self-citationKwan, K. Y., Lam, M. M. S., Krsnik, Ž., Kawasawa, Y. I., Lefebvre, V., & Šestan, N. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806791105 · Cited by 271 · see citing works
Kostovic, I., & Rakic, P. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-01-00025.1984 · Cited by 270 · see citing works
Self-citationChanges in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life
Zecevic, N., Bourgeois, J.-P., & Rakic, P. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90124-7 · Cited by 253 · see citing works
Self-citationMiyoshi, G., & Fishell, G. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq155 · Cited by 230 · see citing works
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
Kalmbach, B. E., Buchin, A., Long, B., Close, J., Nandi, A., Miller, J. A., Bakken, T. E., Hodge, R. D., Chong, P., de Frates, R., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.012 · Cited by 203 · see citing works
Chapter 3 The Developmental Integration of Cortical Interneurons into a Functional Network
Batista‐Brito, R., & Fishell, G. (2009) · Current Topics in Developmental Biology · doi:10.1016/s0070-2153(09)01203-4 · Cited by 223 · see citing works
Transcriptional Architecture of the Primate Neocortex
Bernard, A., Lubbers, L. S., Tanis, K. Q., Luo, R., Podtelezhnikov, A. A., Finney, E. M., McWhorter, M. M. E., Serikawa, K., Lemon, T., Morgan, R., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.002 · Cited by 224 · see citing works
Martínez-Cerdeño, V., Cunningham, C. L., Camacho, J., Antczak, J. L., Prakash, A. N., Cziep, M. E., Walker, A. I., & Noctor, S. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030178 · Cited by 203 · see citing works
A novel cytoarchitectonic area induced experimentally within the primate visual cortex.
Rakic, P., Suñer, I., & Williams, R. W. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.6.2083 · Cited by 208 · see citing works
Self-citationChild Development and Neuroscience.
Nelson, C. A., & Bloom, F. E. (1997) · Child Development · doi:10.1111/j.1467-8624.1997.tb01974.x · Cited by 236 · see citing works
Stancik, E. K., Navarro-Quiroga, I., Sellke, R., & Haydar, T. F. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.6131-09.2010 · Cited by 186 · see citing works
Emerging roles of neural stem cells in cerebral cortex development and evolution
Borrell, V., & Reillo, I. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22013 · Cited by 185 · see citing works
Layer Specification of Transplanted Interneurons in Developing Mouse Neocortex
Valcanis, H., & Tan, S.-S. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05113.2003 · Cited by 175 · see citing works
Evrard, P., Caviness, V. S., Prats-Vinas, J., & Lyon, G. (1978) · Acta Neuropathologica · doi:10.1007/bf00689761 · Cited by 175 · see citing works
Developmental mechanisms channeling cortical evolution
Finlay, B. L., & Uchiyama, R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2014.11.004 · Cited by 163 · see citing works
Evidence for a mechanistic model of cognitive control
Casey, B. J., Durston, S., & Fossella, J. A. (2001) · Clinical Neuroscience Research · doi:10.1016/s1566-2772(01)00013-5 · Cited by 156 · see citing works
Rash, B. G., Duque, A., Morozov, Y. M., Arellano, J. I., Micali, N., & Rakic, P. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1822169116 · Cited by 156 · see citing works
Self-citationRegulation of cerebral cortical neurogenesis by the Pax6 transcription factor
Manuel, M. N., Mi, D., Mason, J. O., & Price, D. J. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00070 · Cited by 153 · 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
Elimination of neurons from the rhesus monkey's lateral geniculate nucleus during development
Williams, R. W., & Rakic, P. (1988) · Journal of Comparative Neurology · doi:10.1002/cne.902720310 · Cited by 124 · see citing works
Self-citationNeuronal Density and Architecture (Gray Level Index) in the Brains of Autistic Patients
Casanova, M. F., Buxhoeveden, D. P., Switala, A. E., & Roy, E. (2002) · Journal of Child Neurology · doi:10.1177/088307380201700708 · Cited by 121 · see citing works
Simmons, P. A., Lemmon, V., & Pearlman, A. L. (1982) · Journal of Comparative Neurology · doi:10.1002/cne.902110308 · Cited by 104 · see citing works
Samuelsen, G. B. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.2.115 · Cited by 95 · see citing works
Segregation of feedforward and feedback projections in mouse visual cortex
Berezovskii, V. K., Nassi, J. J., & Born, R. T. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22675 · Cited by 84 · see citing works
In search of common developmental and evolutionary origin of the claustrum and subplate
Bruguier, H., Suarez, R., Manger, P., Hoerder‐Suabedissen, A., Shelton, A. M., Oliver, D. K., Packer, A. M., Ferran, J. L., García‐Moreno, F., Puelles, L., et al. (2020) · Journal of Comparative Neurology · doi:10.1002/cne.24922 · Cited by 84 · see citing works
Arcila, M. L., Betizeau, M., Cambronne, X. A., Guzman, E., Doerflinger, N., Bouhallier, F., Zhou, H., Wu, B., Rani, N., Bassett, D. S., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.017 · Cited by 80 · 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
Transcriptional Control of Neuronal Migration in the Developing Mouse Brain
Nobrega-Pereira, S., & Marin, O. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp044 · Cited by 57 · see citing works
Anastasiades, P. G., & Butt, S. J. B. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1262-12.2012 · Cited by 49 · see citing works
Gohlke, J. M., Griffith, W. C., & Faustman, E. M. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl151 · Cited by 49 · see citing works
ATRX is required for maintenance of the neuroprogenitor cell pool in the embryonic mouse brain
Ritchie, K., Watson, L. A., Davidson, B., Jiang, Y., & Bérubé, N. G. (2014) · Biology Open · doi:10.1242/bio.20148730 · Cited by 39 · see citing works
Micali, N., Kim, S.-K., Diaz-Bustamante, M., Stein-O’Brien, G., Seo, S., Shin, J.-H., Rash, B. G., Ma, S., Wang, Y., Olivares, N. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107599 · Cited by 31 · see citing works
Self-citationCellular Neuropathology of Tuberous Sclerosis<sup>a</sup>
HUTTENLOCHER, P. R., & WOLLMANN, R. L. (1991) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1991.tb37756.x · Cited by 32 · see citing works
Consequences of trisomy 21 for brain development in Down syndrome
Russo, M. L., Sousa, A. M. M., & Bhattacharyya, A. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00866-2 · Cited by 28 · see citing works
“The generation of the six-layer cortical plate occurs in an inside-out fashion, with the early-born neurons establishing layer 6, then layer 5, and so forth 59 .”
- Authors
- Rakic, P.
- Affiliations
- Boston Children's Hospital (US)
- Corresponding author
- Rakic, Pasko
- ORCID
- Rakic, Pasko
- Venue
- Science
- Published
- 1974-02
- Volume
- 183
- Issue
- 4123
- Pages
- 425-427
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1979952856
- Cited by
- 1,161
- References
- 1
- Citations by year
- 2026: 13 · 2025: 21 · 2024: 19 · 2023: 34 · 2022: 30 · 2021: 28 · 2020: 44 · 2019: 31 · 2018: 36 · 2017: 27 · 2016: 38 · 2015: 29 · 2014: 23 · 2013: 35 · 2012: 26
- FWCI
- 5.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Keywords
- visual cortex, rhesus monkeys, neuronal origin, 3H-thymidine autoradiography, neocortex development
- MeSH terms
- Animals, Haplorhini, Autoradiography, Brain Mapping, Cell Differentiation, Cell Movement, Female, Gestational Age, Macaca, Neurons, Pregnancy, Thymidine, Tritium, Visual Cortex
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