The nigrostriatal pathway in the rat: A single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrixstriatal compartments

Axons from dorsal/ventral tiers of substantia nigra pars compacta (SNc), ve ntral tegmental area (VTA), and retrorubral field (RRF) were traced after i njecting their cell body with biotinylated dextran amine. Fifty-three singl e axons were reconstructed from serial sagittal sections with a camera luci da, and g-opiate receptor immunostaining served to differentiate the strios ome/matrix striatal compartments. Most dorsal tier SNc axons terminate with in the matrix of the dorsal striatum, but their patterns of arborization va ry markedly; some axons innervate one specific matriceal area, whereas othe rs arborize in multiple discontinuous loci. Some dorsal tier SNc axons also project to both striosomes and matrix. Other dorsal tier SNc axons, as wel l as VTA axons, innervate the ventral striatum and send collaterals to stri osomes lying ventrally in the dorsal striatum or to the ventral sector of t he subcallosal streak (SS). Ventral tier SNc axons arborize principally in striosomes, but some ramify in both compartments or in striosomes and the S S. Ventral tier neurons that form deep clusters in substantia nigra pars re ticulata innervate principally the matrix and the SS. The amygdala and vent ral pallidum receive secondary collaterals from striatal axons of dorsal/ve ntral tier neurons or RRF neurons. The subthalamic nucleus receives collate rals from striatal axons of SNc clustered neurons, whereas the globus palli dus gets collaterals from striatal axons of dorsal/ventral tier SNc neurons . These findings reveal that the nigrostriatal pathway is composed of sever al neuronal subsystems, each endowed with a widely distributed axonal arbor ization that allows them to exert a multifaceted influence on striatal and/ or extrastriatal structures.