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

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In the developing CNS, distinct neuronal subtypes are generated by progenitors in a temporally controlled manner during the protracted period of brain development. Spatially controlled allocation of temporally distinct neuronal descendants is fundamental to distinct brain organization, including the formation of layers, columns, and mosaics. The striatum, the largest nucleus of the basal ganglia, which plays crucial roles in the control of motor and cognitive functions, is characterized by mosaic organization of striosome and matrix cells that form a distinct compartment (Pert et al., 1976; Graybiel and Ragsdale, 1978; Herkenham and Pert, 1981; Gerfen, 1984; Mikula et al., 2009). The striosomes form a lattice‐like “connected reticulum” exhibiting a “labyrinthine” structure or patchy cell clusters, whereas the matrix occupies the space between the clusters of striosomes (Pert et al., 1976; Graybiel and Ragsdale, 1978; Herkenham and Pert, 1981; Gerfen, 1984; Mikula et al., 2009). Both the striosome and the matrix consist of medium spiny projection neurons (MSNs) that make up more than 90% of striatal cells. The striosome contains approximately 15% of MSNs, whereas the matrix contains the remainder (Johnston et al., 1990). The striosome and matrix can be distinguished not only by their distinct spatial compartments but by their expression of a unique set of molecular markers and patterns of connectivity (Gerfen et al., 1987; Gerfen, 1989; Graybiel, 1990; Kincaid and Wilson, 1996). Imbalances in the functions of the striosome and matrix are suggested to be involved in many basal ganglia disorders (Crittenden and Graybiel, 2011). Therefore, it is crucial to understand how striosome/matrix mosaic formation is controlled during development.
Many previous studies have suggested that the striosome and matrix cells are generated from the lateral ganglionic eminence (LGE) in a temporally distinct manner. In mice, striosome cells were shown to be generated mostly between embryonic day (E) 11.5 and E13.5, whereas matrix cells are generated mostly from E12.5 onward (Mason et al., 2005). The early‐born striatal cells migrate from the LGE to make up the labyrinthine‐like striosome, whereas the late‐born striatal cells make up the matrix surrounding the striosomes in the striatal mantle layer (ML; Brand and Rakic, 1979; van der Kooy and Fishell, 1987; Song and Harlan, 1994; Mason et al., 2005). This raises the question of how striosome and matrix cells intermingle in the ML and yet remain segregated to form distinct compartments (Groves et al., 1988; Desban et al., 1989; Manley et al., 1994; Mikula et al., 2009). Furthermore, given that the topographical and spatial distribution of this entire “labyrinthine” or “connected reticulum” of the striosomes is conserved, but is still somewhat variable across individuals (Desban et al., 1993; Manley et al., 1994; Mikula et al., 2009), another important question is how the spatial variability of striosomes among individuals can be conferred by the striatum during development.
Here we examine the spatial and temporal regulation of striosome/matrix mosaic formation in the developing striatum and analyze prospectively how the striosome and matrix cells are distributed and migrate within the ML during the late embryonic and early postnatal stages of striatal development. To visualize the presumptive striosome and matrix cells, we employed in vivo electroporation; we labeled the descendants generated from the LGE and then followed these fluorescently labeled descendants afterward. By taking advantage of the fact that striosome and matrix cells have temporally distinct origins, we were able to label these cells as early‐ and late‐born striatal cells, respectively. Furthermore, by combining conventional plasmid‐driven gene expression system with a transposon‐driven gene expression system, we were able to label the striosome and matrix cells using a single electroporation at E10.5.
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