The DOI matches its Crossref record; 70 of the 70 references it cites were found in a registry or an index.
Postnatal shifts of interneuron position in the neocortex of normal and reeler mice: evidence for inward radial migration
Abstract
During development, interneurons migrate to precise positions in the cortex by tangential and radial migration. The objectives of this study were to characterize the net radial migrations of interneurons during the first postnatal week, and to investigate the role of reelin signaling in regulating those migrations. To observe radial migrations, we compared the laminar positions of interneurons (immunoreactive for GABA or Dlx) in mouse neocortex on postnatal days (P) 0.5 and P7.5. In addition, we used bromodeoxyuridine birthdating to reveal the migrations of different interneuron cohorts. To study the effects of reelin deficiency, experiments were performed in reeler mutant mice. In normal P0.5 cortex, interneurons were most abundant in the marginal zone and layer 5. By P7.5, interneurons were least abundant in the marginal zone, and were distributed more evenly in the cortical plate. This change was attributed mainly to inward migration of middle- to late-born interneurons (produced on embryonic days (E) 13.5 to E16.5) from the marginal zone to layers 2-5. During the same interval, late-born projection neurons (non-immunoreactive for GABA or Dlx) migrated mainly outward, from the intermediate zone to upper cortical layers. In reeler cortex, middle- and late-born interneurons migrated from the superplate on P0.5, to the deep cortical plate on P7.5. Late-born projection neurons in reeler migrated in the opposite direction, from the intermediate zone to the deep cortical plate. We conclude that many middle- and late-born interneurons migrate radially inward, from the marginal zone (or superplate) to the cortical plate, during the first postnatal week in normal and reeler mice. We propose that within the cortical plate, interneuron laminar positions may be determined in part by interactions with projection neurons born on the same day in neurogenesis.
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In the citing paper
“Several lines of evidence suggest that the interneurons adopt their laminar distribution in response to cues provided by pyramidal cells.”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Hevner et al., 2004
In the citing paper
“First, interneurons systematically acquire their laminar position after the corresponding pyramidal cells have begun to differentiate into a particular cortical layer (Hevner et al., 2004; Miyoshi and Fishell, 2011; Pla et al., 2006).”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Hevner et al., 2004
In the citing paper
“In the cortex of reeler mice, MGE-derived interneurons are inverted similar to PCs: early-born cells are found ectopically in superficial layers while those born later are found in the deep layers”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [489]
Citations
Cites
Neurons derived from radial glial cells establish radial units in neocortex
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., & Kriegstein, A. R. (2001) · Nature · doi:10.1038/35055553 · Cited by 2,016
A protein related to extracellular matrix proteins deleted in the mouse mutant reeler
D'Arcangelo, G., G. Miao, G., Chen, S.-C., Scares, H. D., Morgan, J. I., & Curran, T. (1995) · Nature · doi:10.1038/374719a0 · Cited by 1,748
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
Interneuron Migration from Basal Forebrain to Neocortex: Dependence on Dlx Genes
Anderson, S. A., Eisenstat, D. D., Shi, L., & Rubenstein, J. L. R. (1997) · Science · doi:10.1126/science.278.5337.474 · Cited by 1,462
Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K., & Kaneko, T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10905 · Cited by 1,277
Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., & Herz, J. (1999) · Cell · doi:10.1016/s0092-8674(00)80782-5 · Cited by 1,261
A long, remarkable journey: Tangential migration in the telencephalon
Marín, Ó., & Rubenstein, J. L. R. (2001) · Nature reviews. Neuroscience · doi:10.1038/35097509 · Cited by 1,077
Asymmetric Inheritance of Radial Glial Fibers by Cortical Neurons
Miyata, T., Kawaguchi, A., Okano, H., & Ogawa, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00420-2 · Cited by 892
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 · cited 1×
“Another molecule that regulates radial migration in the cortex is reelin (D’Arcangelo et al., 1995; Ogawa et al., 1995 ).”
Sussel, L., Marin, O., Kimura, S., & Rubenstein, J. L. R. (1999) · Development · doi:10.1242/dev.126.15.3359 · Cited by 873
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
Self-citationCell Cycle Dependence of Laminar Determination in Developing Neocortex
McConnell, S. K., & Kaznowski, C. E. (1991) · Science · doi:10.1126/science.1925583 · Cited by 787
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
Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G., & Alvarez-Buylla, A. (2001) · Development · doi:10.1242/dev.128.19.3759 · Cited by 722
Two modes of radial migration in early development of the cerebral cortex
Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R., & Pearlman, A. L. (2001) · Nature Neuroscience · doi:10.1038/83967 · Cited by 716
Allendoerfer, K. L., & Shatz, C. J. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.001153 · Cited by 653
Distinct cortical migrations from the medial and lateral ganglionic eminences
Anderson, S. A., Marín, Ó., Horn, C., Jennings, K., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.3.353 · Cited by 651
Caviness, V. S. (1982) · Developmental Brain Research · doi:10.1016/0165-3806(82)90141-9 · Cited by 639
Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex
Hendry, S., Schwark, H. D., Jones, E. G., & Yan, J. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-05-01503.1987 · Cited by 601
Alcántara, S., Ruiz, M., D’Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C., & Soriano, E. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-19-07779.1998 · Cited by 568
Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model
Caviness, V. S., Takahashi, T., & Nowakowski, R. S. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93933-o · Cited by 566
Blaschke, A. J., Staley, K., & Chun, J. J. M. (1996) · Development · doi:10.1242/dev.122.4.1165 · Cited by 532
CXCR4 Regulates Interneuron Migration in the Developing Neocortex
Stumm, R. K., Zhou, C., Ara, T., Lazarini, F., Dubois-Dalcq, M. E., Nagasawa, T., Höllt, V., & Schulz, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05123.2003 · Cited by 450
Mechanisms of programmed cell death in the developing brain
Kuan, C.-Y., Roth, K. A., Flavell, R. A., & RAKIC, P. T. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01581-2 · Cited by 444
Sorting of Striatal and Cortical Interneurons Regulated by Semaphorin-Neuropilin Interactions
Marı́n, O., Yaron, A., Bagri, A., Tessier-Lavigne, M., & Rubenstein, J. L. R. (2001) · Science · doi:10.1126/science.1061891 · Cited by 433
Dynamics of Cell Migration from the Lateral Ganglionic Eminence in the Rat
Carlos, J., López‐Mascaraque, L., & Valverde, F. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06146.1996 · Cited by 403
Origin and Route of Tangentially Migrating Neurons in the Developing Neocortical Intermediate Zone
Tamamaki, N., Fujimori, K. E., & Takauji, R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08313.1997 · Cited by 401
Pesold, C., Impagnatiello, F., Pisu, M. G., Uzunov, D. P., Costa, E., Guidotti, A., & Caruncho, H. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3221 · Cited by 391
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
Apoptosis and Its Relation to the Cell Cycle in the Developing Cerebral Cortex
Thomaidou, D., Mione, M., Cavanagh, J. F. R., & Parnavelas, J. G. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-03-01075.1997 · Cited by 362
Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling
Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T., & Ghosh, A. (2002) · Development · doi:10.1242/dev.129.13.3147 · Cited by 361
Takahashi, T., Goto, T., Miyama, S., Nowakowski, R. S., & Caviness, V. S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10357.1999 · Cited by 333
Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis
Hack, I., Bancila, M., Loulier, K., Carroll, P., & Cremer, H. (2002) · Nature Neuroscience · doi:10.1038/nn923 · Cited by 327
Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation
McConnell, S. K. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-03-00945.1988 · Cited by 311
DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation
Eisenstat, D. D., Liu, J. K., Mione, M., Zhong, W., Yu, G. K., Anderson, S. A., Ghattas, I. R., Puelles, L., & Rubenstein, J. L. R. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991115)414:2 · Cited by 291
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
Local Differences in the Amount of Early Cell Death in Neocortex Predict Adult Local Specializations
Finlay, B. L., & Slattery, M. M. (1983) · Science · doi:10.1126/science.6828866 · Cited by 278
Transcriptional Regulation of Cortical Neuron Migration by POU Domain Factors
McEvilly, R. J., de Diaz, M. O., Schonemann, M. D., Hooshmand, F., & Rosenfeld, M. G. (2002) · Science · doi:10.1126/science.1067132 · Cited by 271
Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons
Sugitani, Y., Nakai, S., Minowa, O., Nishi, M., Jishage, K.-I., Kawano, H., Mori, K., Ogawa, M., & Noda, T. (2002) · Genes & Development · doi:10.1101/gad.978002 · Cited by 259
Beyond Laminar Fate: Toward a Molecular Classification of Cortical Projection/Pyramidal Neurons
Hevner, R. F., Daza, R. A. M., Rubenstein, J. L. R., Stunnenberg, H. G., Olavarría, J. F., & Englund, C. (2003) · Developmental Neuroscience · doi:10.1159/000072263 · Cited by 250
Tan, S., Kalloniatis, M., Sturm, K. S., Tam, P., Reese, B. E., & Faulkner-Jones, B. E. (1998) · Neuron · doi:10.1016/s0896-6273(00)80539-5 · Cited by 238
Neuronal Migration in the Developing Cerebral Cortex: Observations Based on Real-time Imaging
Nadarajah, B. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.6.607 · Cited by 229
Ventricle-directed migration in the developing cerebral cortex
Nadarajah, B., Alifragis, P., Wong, R., & Parnavelas, J. G. (2002) · Nature Neuroscience · doi:10.1038/nn813 · Cited by 224
Cell death and removal in the cerebral cortex during development
Ferrer, I., Soriano, E., del Rı́o, J. A., Alcántara, S., & Auladell, C. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90029-e · Cited by 207
Schmahl, W., Knödlseder, M., Favor, J., & Davidson, D. R. (1993) · Acta Neuropathologica · doi:10.1007/bf00334879 · Cited by 205
Hevner, R. F., Neogi, T., Englund, C., Daza, R. A. M., & Fink, A. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00641-7 · Cited by 202
GABA immunoreactive neurons in rat visual cortex
Meinecke, D. L., & Peters, A. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902610305 · Cited by 196
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
Tanaka, D. H., Nakaya, Y., Yanagawa, Y., Obata, K., & Murakami, F. (2003) · Development · doi:10.1242/dev.00825 · Cited by 169
Apoptosis in the in Vivo Mammalian Forebrain
Dikranian, K. T., Ishimaru, M. J., Tenkova, T. I., Labruyere, J., Qin, Y., Ikonomidou, C., & Olney, J. W. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2001.0411 · Cited by 167
Neurogenic Radial Glial Cells in Reptile, Rodent and Human: from Mitosis to Migration
Weissman, T. A. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.6.550 · Cited by 158
Fairén, A., Cobas, A., & Fonseca, M. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902510105 · Cited by 158
Spreafico, R., Frassoni, C., Arcelli, P., Selvaggio, M., & Biasi, S. D. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903630209 · Cited by 155
Mallamaci, A., Mercurio, S., Muzio, L., Cecchi, C., Pardini, C. L., Gruß, P., & Boncinelli, E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-03-01109.2000 · Cited by 139
In vitro analysis of the origin, migratory behavior, and maturation of cortical pyramidal cells
Hatanaka, Y., & Murakami, F. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10421 · Cited by 131
Marshall, C. A. G., & Goldman, J. E. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09821.2002 · Cited by 122
de Diego, I., Smith‐Fernández, A., & Fairén, A. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00593.x · Cited by 121
Emx1 is a Marker for Pyramidal Neurons of the Cerebral Cortex
Chan, C.-H. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.12.1191 · Cited by 121
Valverde, F., López‐Mascaraque, L., Santacana, M., & Carlos, J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05014.1995 · Cited by 87
Cortical Interneuron Fate Determination: Diverse Sources for Distinct Subtypes?
Xu, Q. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.6.670 · Cited by 82
Genesis of GABA-immunoreactive neurons in the ferret visual cortex
Peduzzi, J. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-03-00920.1988 · Cited by 74
Neurogenesis and Commitment of Corticospinal Neurons inreeler
Polleux, F., Dehay, C., & Kennedy, H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-23-09910.1998 · Cited by 74
A Novel Role for p75NTR in Subplate Growth Cone Complexity and Visual Thalamocortical Innervation
McQuillen, P. S., DeFreitas, M. F., Zada, G., & Shatz, C. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03580.2002 · Cited by 70
The fates of cells generated at the end of neurogenesis in developing mouse cortex
Levers, T. E., Edgar, J. M., & Price, D. J. (2001) · Journal of Neurobiology · doi:10.1002/neu.1056 · Cited by 65
Morozov, Y. M., & Freund, T. F. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00409-3 · Cited by 64
Polleux, F. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.11.1027 · Cited by 52
Hammond, V. E., Howell, B. W., Godinho, L., & Tan, S. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-22-08798.2001 · Cited by 45
Anxiety: at the intersection of genes and experience
Anagnostaras, S., Craske, M. G., & Fanselow, M. S. (1999) · Nature Neuroscience · doi:10.1038/12146 · Cited by 34
Myelin and disorders that affect the formation and maintenance of this sheath
Porter, B. E., & Tennekoon, G. I. (2000) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/(sici)1098-2779(2000)6:1 · Cited by 14
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“First, interneurons systematically acquire their laminar position after the corresponding pyramidal cells have begun to differentiate into a particular cortical layer (Hevner et al., 2004; Miyoshi and Fishell, 2011; Pla et al., 2006).”
Metadata
- Authors
- Hevner, R. F., Daza, R. A. M., Englund, C., Kohtz, J., & Fink, A.
- Affiliations
- University of Washington (US)
- Northwestern University (US)
- Corresponding author
- Hevner, R.F
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2004-01
- Volume
- 124
- Issue
- 3
- Pages
- 605-618
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W1970617579
- Cited by
- 180
- References
- 70
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2022: 4 · 2021: 5 · 2020: 7 · 2019: 8 · 2018: 7 · 2017: 13 · 2016: 5 · 2015: 12 · 2014: 7 · 2013: 13 · 2012: 8
- FWCI
- 3.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (7k08ns001973-06)
- National Institute of Neurological Disorders and Stroke (K08 NS01973)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD044745)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Keywords
- interneuron migration, radial migration, in-migration, Reelin signaling, reeler mutant mice, neocortex, cortical lamination, marginal zone, cortical plate, projection neurons, GABAergic interneurons, postnatal development, neurogenesis
- MeSH terms
- Reelin Protein, Animals, Animals, Newborn, Bromodeoxyuridine, Cell Differentiation, Cell Division, Cell Movement, Cerebral Cortex, Fetus, gamma-Aminobutyric Acid, Immunohistochemistry, Interneurons, Mice, Neurologic Mutants, Nerve Tissue Proteins, Nervous System Malformations, Neural Inhibition, Neural Pathways, Serine Endopeptidases, Transcription Factors, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Apoptosis, Homeodomain Proteins, Cell Lineage, Body Patterning, Mice
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