Current Biology
Volume 25, Issue 19, 5 October 2015, Pages 2466-2478
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Article
Migration Speed of Cajal-Retzius Cells Modulated by Vesicular Trafficking Controls the Size of Higher-Order Cortical Areas

https://doi.org/10.1016/j.cub.2015.08.028Get rights and content
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Highlights

  • Subtype-specific migration kinetics determine CRs cortical distributions

  • Inhibiting VAMP3 increases migration speed, but not directionality, of CR subtypes

  • VAMP3-dependent vesicular trafficking regulates CR cortical dispersion

  • Altered CRs distribution changes the size and wiring of higher-order cortical areas

Summary

In the neocortex, higher-order areas are essential to integrate sensory-motor information and have expanded in size during evolution. How higher-order areas are specified, however, remains largely unknown. Here, we show that the migration and distribution of early-born neurons, the Cajal-Retzius cells (CRs), controls the size of higher-order areas in the mouse somatosensory, auditory, and visual cortex. Using live imaging, genetics, and in silico modeling, we show that subtype-specific differences in the onset, speed, and directionality of CR migration determine their differential invasion of the developing cortical surface. CR migration speed is cell autonomously modulated by vesicle-associated membrane protein 3 (VAMP3), a classically non-neuronal mediator of endosomal recycling. Increasing CR migration speed alters their distribution in the developing cerebral cortex and leads to an expansion of postnatal higher-order areas and congruent rewiring of thalamo-cortical input. Our findings thus identify novel roles for neuronal migration and VAMP3-dependent vesicular trafficking in cortical wiring.

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