The DOI matches its Crossref record; 12 of the 12 references it cites were found in a registry or an index.
Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods
Abstract
Methacrylate‐embedded sections and short‐survival thymidine radiograms of the hippocampal dentate gyrus were examined in perinatal and postnatal rats in order to trace the site of origin and migration of the precursors of granule cells and study the morphogenesis of the granular layer. The densely packed, spindle‐shaped cells of the secondary dentate matrix (a derivative of the primary dentate neuroepithelium) stream in a subpial position towards the granular layer of the internal dentate limb during the perinatal and early postnatal periods. By an accretionary process, the crest of the granular layer forms on day E21 and on the subsequent days the granular layer of the internal dentate limb expands progressively in a lateral direction. Granule cells differentiation, as judged by the transformation of polymorph, darkly staining small cells into rounder, lightly staining larger granule cells, follows the same gradient from the external dentate limb to the internal dentate limb. The secondary dentate matrix is in a process of dissolution by day P5. This matrix is the source of what will later become the outer shell of the granular layer composed of early generated granule cells. The thicker inner shell of the granular layer, formed during the infantile and juvenile periods, derives from an intrinsic, tertiary germinal matrix. On day E22, the dentate migration of the secondary dentate matrix becomes partitioned into two components: (a) the subpial component of extradentate origin, referred to in this context as the first dentate migration, and (b) the second dentate migration. The latter is distributed in the basal polymorph layer throughout the entire dentate gyrus and is henceforth recognized as the tertiary dentate matrix. The tertiary dentate matrix is prominent between days P3 and P10. It is postulated that the great increase in granule cell population during the infantile period is principally due to cells derived from this intrinsic matrix of the dentate gyrus. Between days P20 and P30 the tertiary dentate matrix disappears in the basal polymorph layer and henceforth proliferative cells become largely confined to the subgranular zone at the base of the granular layer. The subgranular zone is the source of granule cells produced during the juvenile and adult periods.
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“reduction in PTB triggered radial glial-like cells to convert into new granular neurons through what appears to be the typical developmental process by which new hippocampal neurons mature during development39 and in young adult animals40.”
From Therapeutically viable generation of neurons with antisense oligonucleotide suppression of PTB (2021) · cites this paper as [39]
Citations
Cites
Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats
Altman, J., & Das, G. D. (1965) · Journal of Comparative Neurology · doi:10.1002/cne.901240303 · Cited by 3,592
Self-citationBayer, S. A. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901900107 · Cited by 913
Self-citationAutoradiographic investigation of cell proliferation in the brains of rats and cats
Altman, J. (1963) · The Anatomical Record · doi:10.1002/ar.1091450409 · Cited by 623
Self-citationTime of neuron origin in the hippocampal region. An autoradiographic study in the mouse.
Angevine, J. B. (1965) · PubMed · Cited by 476
Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections
Stanfield, B. B., & Trice, J. (1988) · Experimental Brain Research · doi:10.1007/bf00250261 · Cited by 431
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010302 · Cited by 401
Self-citationBayer, S. A. (1982) · Experimental Brain Research · doi:10.1007/bf00238626 · Cited by 285
Self-citationEckenhoff, M. F., & RAKIC, P. T. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902230102 · Cited by 239
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010303 · Cited by 198
Self-citationOn the number of neurons in the dentate gyrus of the rat
Boss, B. D., Peterson, G. M., & Cowan, W. M. (1985) · Brain Research · doi:10.1016/0006-8993(85)90257-4 · Cited by 178
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Chiesa, M. (2018) · theses.fr (ABES) · doi:10.70675/6ef32b4fzb74az4b06zb8edz92268c28d542
Etude du développement des neurones granulaires du gyrus denté : morphogénèse et régulation par Rnd2
Kerloch, T. (2018) · theses.fr (ABES) · doi:10.70675/b55bca9fz2395z4dc2za985zbc6c617f23ed
Génétique et physiopathologie du syndrome de Lowe, analyse des aspects neurologiques
Héritier, A. (2019) · theses.fr (ABES) · doi:10.70675/de6a261fz5927z43bdza3cez77bae3ad1666
Holubová-Kroupová, A., & Šlamberová, R. (2026) · Physiology & Behavior · doi:10.1016/j.physbeh.2026.115380
Spatial and Molecular Progression of Neural Progenitor Cells in the Developing Human Dentate GyrusPreprint
Pastor-Alonso, O., Heffel, M. G., Baig, M. S., Harris, J., González-Granero, S., Li, S., Beccari, S., Chu, J. S. F., Lambing, H., Lu, I.-L., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.06.730648
Isolation of postnatal human neural stem cellsPreprint
Liu, D. D., Eastman, A. E., Womack-Gambrel, N. L., Kim, C. N., He, J. Q., Raj, S., Reilly, E. E., Sinha, R., Uchida, N., Chau, K., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.11.731596
Czarzasta, K., Bogacki-Rychlik, W., Joniec‐Maciejak, I., Machaj, E., Momot, K., Segiet, A., & Sajdel, E. M. (2026) · Scientific Reports · doi:10.1038/s41598-026-47910-y · Cited by 1
Tirado-Melendro, P., Li, L., Medina-Menéndez, C., Jurado‐Angulo, P., Rodríguez‐Martín, P., García-Redondo, L., Bilińska, K., & Morales, A. V. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1876208
Early spinogenesis in postnatally-born hippocampal granule cells
Frey, L., Kirscht, S., Ebert, J., Hanauske, T., Deller, T., Schwarzacher, S. W., & Jungenitz, T. (2026) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2026.1899044
Scrable, H. J., & Ashrafzadeh‐Kian, S. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7696-2_25
Lateralization of the developing rat hippocampal formation
Gross, A. L. (2011) · UNM’s Digital Repository (University of New Mexico)
Metadata
- Authors
- Altman, J., & Bayer, S. A.
- Affiliations
- Purdue University West Lafayette (US)
- Indiana University – Purdue University Indianapolis (US)
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1990-11-15
- Volume
- 301
- Issue
- 3
- Pages
- 365-381
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2006624547
- Cited by
- 819
- References
- 12
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 9 · 2023: 9 · 2022: 18 · 2021: 17 · 2020: 24 · 2019: 29 · 2018: 28 · 2017: 37 · 2016: 33 · 2015: 35 · 2014: 31 · 2013: 35 · 2012: 39
- FWCI
- 3.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- hippocampal granule cells, granule cell precursors, dentate gyrus, subgranular zone, perinatal development, postnatal development, cell migration, granule cell differentiation
- MeSH terms
- Aging, Animals, Autoradiography, Cell Differentiation, Cell Division, Cell Movement, Gestational Age, Hippocampus, Morphogenesis, Rats, Inbred Strains, Thymidine, Tritium, Rats
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