Distinct migratory behaviors of striosome and matrix cells underlying the mosaic formation in the developing striatum

ABSTRACT The striatum, the largest nucleus of the basal ganglia controlling motor and cognitive functions, can be characterized by a labyrinthine mosaic organization of striosome/matrix compartments. It is unclear how striosome/matrix mosaic formation is spatially and temporally controlled at the cellular level during striatal development. Here, by combining in vivo electroporation and brain slice cultures, we set up a prospective experimental system in which we differentially labeled striosome and matrix cells from the time of birth and followed their distributions and migratory behaviors. Our results showed that, at an initial stage of striosome/matrix mosaic formation, striosome cells were mostly stationary, whereas matrix cells actively migrated in multiple directions regardless of the presence of striosome cells. The mostly stationary striosome cells were still able to associate to form patchy clusters via attractive interactions. Our results suggest that the restricted migratory capability of striosome cells may allow them to cluster together only when they happen to be located in close proximity to each other and are not separated by actively migrating matrix cells. The way in which the mutidirectionally migrating matrix cells intermingle with the mostly stationary striosome cells may therefore determine the topographic features of striosomes. At later stages, the actively migrating matrix cells began to repulse the patchy clusters of striosomes, presumably enhancing the striosome cluster formation and the segregation and eventual formation of dichotomous homogeneous striosome/matrix compartments. Overall, our study reveals temporally distinct migratory behaviors of striosome/matrix cells, which may underlie the sequential steps of mosaic formation in the developing striatum. J. Comp. Neurol. 525:794–817, 2017. © 2016 Wiley Periodicals, Inc.