Abstract
The mammalian neocortex is characterized as a six-layered laminar structure, in which distinct types of pyramidal neurons are distributed coordinately during embryogenesis. In contrast, no other vertebrate class possesses a brain region that is strictly analogous to the neocortical structure. Although it is widely accepted that the pallium, a dorsal forebrain region, is specified in all vertebrate species, little is known of the differential mechanisms underlying laminated or non-laminated structures in the pallium. Here we show that differences in patterns of neuronal specification and migration provide the pallial architectonic diversity. We compared the neurogenesis in mammalian and avian pallium, focusing on subtype-specific gene expression, and found that the avian pallium generates distinct types of neurons in a spatially restricted manner. Furthermore, expression of Reelin gene is hardly detected in the developing avian pallium, and an experimental increase in Reelin-positive cells in the avian pallium modified radial fiber organization, which resulted in dramatic changes in the morphology of migrating neurons. Our results demonstrate that distinct mechanisms govern the patterns of neuronal specification in mammalian and avian pallial development, and that Reelin-dependent neuronal migration plays a critical role in mammalian type corticogenesis. These lines of evidence shed light on the developmental programs underlying the evolution of the mammalian specific laminated cortex.
Highlights
The mammalian cortex is one of the most intricate brain structures in which distinct types of neurons are located in specific laminar positions enabling their elaboration into highly orchestrated neuronal circuits
To compare specific neuronal subtypes between the mammalian and avian pallium, we first focused on several markers that are expressed in laminar specific subtypes of mammalian cortical neurons
In the developing quail embryos, we did not detect Reelin expression in the dorsal and lateral pallium, a small number of Reelin-positive cells were localized on the surface of the medial pallium and the ventral part of the telencephalon (Fig. 1B, 1C and Figure S1), as reported previously in chick embryos [21]
Summary
The mammalian cortex is one of the most intricate brain structures in which distinct types of neurons are located in specific laminar positions enabling their elaboration into highly orchestrated neuronal circuits. (reviewed in [1]). All of pyramidal neurons are generated from two proliferative areas in the cortical primordium, the ventricular and subventricular zones. Neuronal progenitors in the ventricular zone, namely neuroepithelial cells or radial glial cells possess long processes that extend from the ventricular wall to the pial surface. These processes called radial glial fibers play essential roles for guiding neurons from the proliferative areas toward the pial surface (reviewed in [3,4]). Different types of pyramidal neurons are sequentially born to be fated to specific laminar positions. Spatio-temporaly cooperative regulation of neuronal specification and migration is essential for construction of the highly laminated mammalian cortex (reviewed in [5,6,7])
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