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Marginal zone
Cortical plate
Cajal-
Retzius
cells
Pre-plate
Sub-
plate
Intermediate zone
VZ
VZ
FIGURE 3.15 Histogenesis in the cerebral cortex proceeds through three stages. In the first stage of histo-
genesis, the wall of the cerebral cortex is made up of the progenitor cells, which occupy the ventricular zone
(VZ). In the next stage of development, the first neurons exit the cell cycle (red) and accumulate in the preplate,
adjacent to the pial surface. The neurons of the preplate can be divided into the more superficial Cajal-Retzius
cells and the subplate cells. In the next stage of cortical histogenesis, newly generated neurons (red) migrate
along radial glial fibers to form a layer between the Cajal-Retzius cells and the subplate. This layer is called the
cortical plate, and the majority of the neurons in the cerebral cortex accumulate in this layer.
migration. However, the accumulation of neurons
within the cortical plate results in a marked increase in
cortical thickness. As a result, the processes of progeni-
tor cells no longer are able to extend to the external
surface of the cortex. Nevertheless, the newly gener-
ated cortical neurons still migrate primarily in a radial
direction. How is this accomplished? To guide the
newly generated cortical neurons to their destinations,
a remarkable set of cells, known as radial glia , provide a
scaffold. These glial cells have long processes that
extend from the ventricular zone all the way to the pial
surface. They form a scaffold that neurons migrate
along. Serial section electron microscopic studies by
Pasko Rakic first clearly demonstrated the close associ-
ation of migrating neurons with the radial glial cells
in the cerebral cortex (Figure 3.16). The migrating
neurons wrap around the radial glial processes like a
person climbing a pole. In recent years, it has been
possible to directly observe the process of neuronal
migration in vitro using dissociated cell cultures
(Edmonson and Hatten, 1987) or cortical slices
(O¢Rourke et al., 1995). These studies have confirmed
that newly generated neurons migrate along the glial
cells and that the process is saltatory, with migrating
neurons frequently starting and stopping along the way.
The next phase of cortical histogenesis is charac-
terized by the gradual appearance of defined layers
within the cortical plate. As increasing numbers of
newly generated neurons migrate from the ventricular
zone into the cortical plate, they settle in progressively
more peripheral zones. Meanwhile, the earlier-generated
neurons are differentiating. Thus, later-generated
neurons migrate past those generated earlier. This
results in an inside-out development of cortical layers
(Figure 3.17). Richard Sidman (Angevine and Sidman,
1961) used the 3H-thymidine birthdating technique
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