Genesis and migration patterns of neurons forming the patch and matrix compartments of the rat striatum.

ABSTRACT

The mammalian striatum is divided into two compartments, the patch (or striosome) and the matrix, which differ on the basis of several cytochemical markers, connection patterns, and time of neurogenesis. In the rat, the patch compartment consists of clusters of neurons isolated by matrix neurons; included in the patch compartment is a rim of neurons subjacent to the corpus callosum and external capsule, called the subcallosal streak. To study the genesis and migration patterns of striatal neurons forming these compartments, we injected pregnant rats with 5-bromo-2'-deoxyuridine (BrdU, which is incorporated into DNA during S-phase mitosis) on embryonic (E) day 14, to label patch neurons, or on E19, to label matrix neurons. Embryos were sacrificed at intervals after injection, for detection of BrdU by immunocytochemistry. Cells labeled at E14 were distributed fairly uniformly in the differentiated portion of the caudate-putamen through E19. However, by the day of birth (P0), E14-labeled cells were clustered into patches and the subcallosal streak. Using double immunocytochemistry for BrdU and for the patch marker substance P, we demonstrated a caudal-rostral gradient in the birth dates of neurons in the patch compartment; E14-labeled cells occupied substance P-labeled patches at the level of the posterior limb of the anterior commissure, but patches further rostral were nearly devoid of E14-labeled cells. The distance between the lateral ventricle and the nearest E14-labeled cells was greater on E19 than on E16 or on P0, suggesting secondary movement of early-born neurons during the process of cluster formation. Neurons labeled at E19 formed the matrix surrounding clusters of unlabeled cells, except in the nucleus accumbens (ventral striatum), where E19-labeled cells formed clusters. The data suggest that the uniformly-distributed population of early-born neurons is disrupted by the invasion of later-born (matrix) neurons, forcing the early-born neurons into clusters which are displaced toward the ventricular surface to form the patch compartment. Early-born neurons adjacent to the external capsule are not displaced, forming the subcallosal streak.