Morphological and physiological properties of parvalbumin- and calretinin-containing γ-aminobutyric acidergic neurons in the substantia nigra

Evidence for the existence of different populations of gamma-aminobutyric acid (GABA)-ergic neurons in the substantia nigra comes partially from anatomical studies, which have shown there to be little if any overlap between the calcium-binding proteins parvalbumin and calretinin in individual neurons, suggesting that these may represent neuronal subtypes with distinct electrophysiological and/or anatomical properties. We obtained whole-cell recordings from neurons in the substantia nigra pars reticulata in rat brain slices and labeled them with biocytin, followed by immunocytochemical staining for parvalbumin and calretinin. In other cases, neurons were retrogradely labeled from the thalamus or tectum and immunocytochemically identified to determine their projection sites. Intracellularly stained neurons were found to have a variety of somatic sizes and shapes. Reconstructions revealed that all parvalbumin- and calretinin-positive neurons issued at least one axon collateral, which ramified within the substantia nigra pars reticulata and/or pars compacta. Local collaterals were of medium caliber and branched modestly, expressing many long, smooth segments that then issued numerous en passant or terminal boutons, consistent with previous in vivo studies. There were no clear differences in the electrophysiological or morphological properties of neurons expressing parvalbumin or calretinin. Retrograde tracing experiments revealed that both parvalbumin- and calretinin-containing neurons project nonpreferentially to the thalamus or tectum. In sum, the parvalbumin- and calretinin-containing GABAergic neurons of the substantia nigra pars reticulata cannot be differentiated on the basis of their electrophysiological properties, morphological properties, or target nuclei, and both parvalbumin- and calretinin-containing projection neurons issue local axon collaterals that arborize within the substantia nigra.