The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat.

The aim of the present study was to provide a detailed account of the axonal branching pattern of striatal projection neurons in the rat. Seventy-seven striatofugal neurons were singly labeled following juxtacellular injection of biotin dextran amine. Their axons were entirely reconstructed along the sagittal plane with the help of a light microscope equipped with a camera lucida. The major findings of this study can be summarized as follows, (1) the striatofugal system originates from medium-sized spiny neurons that project only to globus pallidus (GP, type I, 36.4%), to both GP and substantia nigra pars reticulata (SNr, type II, 26%), or to globus pallidus, entopeduncular nucleus (EP) and SNr (type III, 37.6%); (2) the striatofugal system displays a high degree of axonal collateralization; about two-thirds of its axons arborize into two or three striatal target structures; (3) virtually all striatofugal axons send collaterals to the GP and none project exclusively to the EP and or SNr; (4) the three types of striatal projection neurons share similar somatodendritic morphology and have no preferential distribution in the dorsal striatum. These data, together with those of previous investigations, indicate that the striatofugal system can no longer be considered to be a simple dual (direct indirect) projection system. Instead, it stands out as a complex and widely distributed neuronal network whose elements are endowed with a highly patterned set of axon collaterals, which allows them to control in an exquisitely precise manner the flow of information along the main axis of the basal ganglia.