Abstract

Despite recent studies elucidating the molecular mechanisms underlying cortical patterning and map formation, very little is known about how the embryonic pallium expands ventrally to form the future cortex and the nature of the underlying force-generating events. We find that neurons born at embryonic day 10 (E10) in the mouse dorsal pallium ventrally stream until E13, thereby superficially spreading the preplate, and then constitute the subplate from E14. From E11 to E12, the preplate neurons migrate, exerting pulling and pushing forcesat the process and the soma, respectively. At E13, they are morphologically heterogeneous, with ∼40% possessing corticofugal axons, which are found to be in tension. Ablation of these E10-born neurons attenuates both deflection of radial glial fibers (by E13) and extension of the cortical plate (by E14), which should occur ventrally, and subsequently shrinks the postnatal neocortical map dorsally. Thus, the preplate stream physically primes neocortical expansion and arealization.

Highlights

  • Mammalian neocortex exhibits a disproportionally ‘‘luxurious’’ representation of somatotopies in its lateral region

  • Clonal analyses revealed a greater tangential dispersion of neurons in the lateral part of the growing neocortex than in the medial part (Tan et al, 1995; Gao et al, 2014). One explanation for this ventral neocortical expansion is that radial glial fibers, which are used for neuronal guidance (Rakic, 1972), exhibit an extensively curving and divergent alignment pattern in the lateral part (Misson et al, 1988, 1991) (Figure 1B), which can be coupled with tangential translocations of neurons from one radial fiber (RF) to another (O’Rourke et al, 1992; Tabata and Nakajima, 2003)

  • Recent studies have reported that some SP neurons come from an extracortical origin by a medial-to-lateral influx (Pedraza et al, 2014; Garcıa-Moreno et al, 2018) and that a fraction of neurons born in the ventricular zone (VZ) of the pallium and the palliostriatal interface migrate ventrally to contribute to the lateral olfactory tract (LOT) area, olfactory cortex, amygdala, striatum, or other forebrain structures (Tomioka et al, 2000; Hamasaki et al, 2001; Hirata et al, 2002; Remedios et al, 2007; GarcıaMoreno et al, 2008; Cocas et al, 2009; Pombero et al, 2011)

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Summary

Graphical Abstract

Embryonic radial glial fibers that guide most neocortical neurons are ventrally deflected near their terminal, contributing to further expansion of the neocortical area. Saito et al demonstrate that this fiber deflection is induced physically by a previously unrecognized ventral stream of the earliest generated preplate neurons. 2019, Cell Reports 29, 1555–1567 November 5, 2019 a 2019 The Author(s).

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