In the developing nervous system, two modes of migration have been identified: radial and tangential. Radial migration is the principal mode of migration in the developing cerebral cortex, although the GABA (γ-aminobutyric acid)-expressing interneurons, which arise in the ventral telencephalon, migrate tangentially into the cortex.
Layers II–VI of the mammalian cortex are generated in an 'inside-out' sequence, such that early-born cells reside in the deepest layers, whereas later-born cells migrate past the existing layers to form the superficial layers.
Radially migrating neurons adopt two separate modes of movement: somal translocation during the early stages of corticogenesis; and glia-guided migration during the later stages, when the cerebral wall is considerably thicker.
Evidence for somal translocation came from the reeler mouse and from other mutants that have abnormal cortical lamination. Although these mutations disrupt glia-guided migration, the preplate forms normally, indicating that another mode of radial migration is required for the early stages of cortical lamination.
Translocation might be an older mode of movement in the evolution of the cerebral cortex for the transfer of preplate and early cortical-plate neurons, whereas glia-guided migration might have evolved to guide cells across more complex paths during late corticogenesis.
Little is known about how tangentially migrating interneurons integrate into specific cortical layers. A recent study has shown that they migrate towards the cortical ventricular zone, a mode of movement termed 'ventricle-directed migration'. Here, they might receive layer information that is essential for their correct integration. The next challenge will be to establish where they acquire spatial information, and what signals guide them to their correct positions.
The conventional scheme of cortical formation shows that postmitotic neurons migrate away from the germinal ventricular zone to their positions in the developing cortex, guided by the processes of radial glial cells. However, recent studies indicate that different neuronal types adopt distinct modes of migration in the developing cortex. Here, we review evidence for two modes of radial movement: somal translocation, which is adopted by the early-generated neurons; and glia-guided locomotion, which is used predominantly by pyramidal cells. Cortical interneurons, which originate in the ventral telencephalon, use a third mode of migration. They migrate tangentially into the cortex, then seek the ventricular zone before moving radially to take up their positions in the cortical anlage.
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Research in our laboratory was supported by the Wellcome Trust.
CP, cortical plate; IZ, intermediate zone; PZ, proliferative (or ventricular) zone. Arrows point to cell bodies.
In the first movie, the arrowhead points to the tip of the leading process. CP, cortical plate; VZ, ventricular zone.
The small arrow points to the tip of the leading process of the cell as it rapidly advances towards the ventricular surface (bottom). The large arrow points to a growing trailing process that will later become the leading process as the cell changes direction and moves towards the pial surface. CP, cortical plate; IZ, intermediate zone; VZ, ventricular zone.
Encyclopedia of Life Sciences
- CAJAL–RETZIUS CELL
A transient pioneer neuron that is located in layer I of the developing neocortex and hippocampus.
- X-INACTIVATED MOSAICS
Based on the process of X-linked gene inactivation, the analysis of X-linked transgenic markers (for example, LacZ) provides a method to distinguish between clonally related cell populations in the developing brain.
- GOLGI STAINING
A histological staining technique that involves impregnating the tissue with silver nitrate. This labels a random subset of neurons, allowing the entire cell and its processes to be visualized.
A mutant mouse with a phenotype that is characterized by tremors, dystonia and ataxia.
A lipophilic carbocyanine dye that emits an intense fluorescence when incorporated into cell membranes. It is commonly used to track cell migration, or for the retrograde or anterograde tracing of axons. It can be used on both live and fixed tissue.
- RHO GTPASE
A Ras-related GTPase that is involved in controlling the polymerization of actin.
- DYNEIN MOTOR
A microtubule-based molecular motor that moves towards the minus end of microtubules.
Literally meaning 'smooth brain', lissencephaly is a human brain disorder that is characterized by absence or reduction of the cerebral convolutions.
- MILLER–DIEKER SYNDROME
A form of lissencephaly that is accompanied by dysmorphic facial features.
A calcium-binding protein that is used as a marker of preplate neurons.
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Nadarajah, B., Parnavelas, J. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3, 423–432 (2002). https://doi.org/10.1038/nrn845
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