Pattern formation in the striatum: developmental changes in the distribution of striatonigral projections

The mammalian striatum (the major subcortical structure in the telencephalon) can be divided into two compartments, the patch and the matrix, on the basis of various neurochemical and hodological markers expressed in the adult. The primary efferent target of striatal neurons is the substantia nigra. We have previously shown that the patch compartment sends projections to the substantia nigra embryonically; whereas the matrix does not form a similar projection until the early postnatal period (Fishell and van der Kooy, J. Neurosci., 7 (1987) 1969-1978). The projection of patch neurons to the substantia nigra is the earliest developmental marker for the patch compartment. Here we ask about the early distribution of patch projections and their possible relation to striatal compartmentalization. Embryonic anterograde axonal tracing of the striatonigral pathway can take advantage of the temporal separation of patch versus matrix projections to reveal the terminal distribution of patch striatonigral neurons independent of the nigral terminal distribution from the striatal matrix. The anterograde tracer rhodamine isothiocyanate was shown in a model system to persist in labeled neurons for more than a week, but to be available for uptake into these neurons for a few days after injection at the most. These properties of rhodamine isothiocyanate were combined experimentally with short and long term survival periods. This allowed assessment of the changing developmental distribution of nigral fibers from specifically the striatal patch compartment. In all experimental cases the anterogradely labeled sections of the substantia nigra were also stained with antibodies to tyrosine hydroxylase, which permitted differentiation of the dopamine cell rich pars compacta from the dopamine cell poor pars reticulata. The results show that in the adult the majority of patch and matrix striatonigral projections are confined to the substantia nigra pars reticulata. Furthermore, their fiber distribution within the pars reticulata is overlapping rather than complementary. Most interestingly, in the late embryonic period (most noticeably at embryonic day 19) there is a marked overlap between patch striatonigral fibers and nigral dopamine perikarya. By early postnatal times, when the matrix compartment begins to form its striatonigral projection, the overlap of patch striatonigral fibers and dopamine cells has largely disappeared. The results suggest that a transient interaction between patch striatonigral fibers and dopamine neurons (which is concomitant with the formation of striatal compartments), may be an important developmental event in the phenotypic maturation of striatal patch/matrix organization.