Mode of cell migration to the superficial layers of fetal monkey neocortex
Abstract
Golgi and electronmicroscopic methods were used to define the shapes and intercellular relationships of cells migrating from their sites of origin near the ventricular surface across the intermediate zone to the superficial neocortical layers of the parietooccipital region in the brains of 75‐ to 97‐day monkey fetuses. After mitotic division in either ventricular or subventricular zones, the cells enter the intermediate zone and assume an elongated bipolar form oriented toward the cortical plate. The leading processes, 50 to 70 μ long, are irregular cytoplasmic cylinders containing prominent Golgi apparatus, mitochondria, microtubules, ribosomal rosettes, immature endoplasmic reticulum and occasional centrioles. They usually terminate in several attenuated expansions, the longest one oriented toward the cortical plate. The trailing processes are more slender, relatively uniform in caliber and display few organelles. Throughout the 3500 μ pathway across the intermediate zone the migrating cells are apposed to elongated, radially oriented, immature glial processes which span the full thickness of the cerebral wall. Most of the perikarya of these glial cells in the younger specimens lie in the ventricular or subventricular zones, but in older fetuses of this series many are found in the intermediate zone. The main characteristics of these fibers are: elongated cylindrical form contaiing numerous microtubules; electronlucent cytoplasmic matrix; short lamellate expansions protruding at right angles from the segment of the fiber which runs through the intermediate zone; and terminal endfeet joined at the pial surface to form a continuous sheet coated externally with basement membrane. It is suggested that glial radial fibers provide guidelines for cell migration through the complex mixture of closely packed cell processes and cell bodies that compose the developing cerebral wall. Strong surface affinity between radial fiber and migrating cell is suggested in regions where both follow precisely the same curving course from subventricular to intermediate zones and also in areas where large extracellular spaces separate other cells and processes but in which migrating cells and radial fibers remain closely paired nonetheless. Specific affinity between them is implied in the failure of migrating cells to follow any of the myriad differently‐oriented processes they encounter. Several generations of postmitotic cells appear to migrate along the same radial fiber, a developmental mechanism that would allow for the vertical cell columns of adult neocortex.
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After symmetric divisions, radial glia divide asymmetrically, generating postmitotic excitatory neurons that migrate to their final location in the cerebral cortex by using the basal process of the radial glial cell as a scaffold.
“After this period of symmetric divisions, these progenitor cells — also known as radial glia — divide asymmetrically, generating postmitotic excitatory neurons that will migrate to their final location in the cerebral cortex by using the basal process of the radial glial cell as a scaffold55–58.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [55]
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- Authors
- Rakic, P.
- Affiliations
- Harvard University (US)
- Corresponding author
- Rakic, Pasko
- ORCID
- Rakic, Pasko
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1972-05
- Volume
- 145
- Issue
- 1
- Pages
- 61-83
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2077630079
- Cited by
- 2,170
- References
- 1
- Citations by year
- 2026: 20 · 2025: 28 · 2024: 31 · 2023: 35 · 2022: 37 · 2021: 39 · 2020: 65 · 2019: 53 · 2018: 49 · 2017: 52 · 2016: 54 · 2015: 49 · 2014: 50 · 2013: 69 · 2012: 55
- FWCI
- 6.52
- 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
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- neuronal migration, intermediate zone, neocortex development, radial glial fibers, cortical plate, ventricular zone, subventricular zone, Golgi apparatus, microtubules, glial processes, cortical columns
- MeSH terms
- Animals, Haplorhini, Cell Differentiation, Cell Movement, Cerebral Cortex, Cerebral Ventricles, Female, Gestational Age, Macaca, Microscopy, Electron, Neurons, Pregnancy, Telencephalon
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