Distinct regulations by septide and the neurokinin-1 tachykinin receptor agonist [Pro(9)]substance P of the N-methyl-D-aspartate-evoked release of dopamine in striosome- and matrix-enriched areas of the rat striatum

The effects of septide (a short substance P C-terminal analogue) and of the neurokinin-1 receptor agonist [Pro(9)]substance P on the N-methyl-D-aspartate (50 mu M)-evoked release of [H-3]dopamine (continuously synthesized from [H-3]tyrosine) were investigated in the absence or the presence of the selective neurokinin-1 receptor antagonist RP 67580 in selected striosome- and matrix-enriched areas of the rat striatum. Experiments were performed in vitro using a microsuperfusion procedure described previously. At a concentration of 0.1 mu M, septide and [Pro(9)]substance P stimulated the spontaneous release of [H-3]dopamine in striosome-enriched areas similarly. However, in this compartment, these peptides induced larger and opposite effects on the N-methyl-D-aspartate (50 mu M)-evoked release of [H-3]dopamine (estimated in the absence of magnesium). Indeed, septide markedly enhanced the N-methyl-D-aspartate response, while [Pro(9)]substance P largely reduced the N-methyl-D-aspartate-evoked release of [H-3]dopamine. Septide also enhanced the N-methyl-D-aspartate response in the matrix, but [Pro(9)]substance P was without effect. When used alone, at 0.1 or 1 mu M, RP 67580 reduced by about 33% the N-methyl-D-aspartate-evoked release of [H-3]dopamine in striosome-enriched areas. In contrast, in the matrix, the N-methyl-D-aspartate response was enhanced in the presence of a low concentration of the antagonist, while the higher concentration was ineffective. In striosomes, the reducing effect of [Pro(9)]substance P and the enhancing action of septide on the N-methyl-D-aspartate response were respectively blocked in the presence of low and high concentrations of RP 67580, while the stimulatory effect of septide on the N-methyl-D-aspartate response in the matrix was prevented with both concentrations of the neurokinin-1 receptor antagonist. Finally, the co-application of [Pro(9)]substance P (0.1 mu M) with septide (0.1 mu M) abolished the enhancing effect of septide on the N-methyl-D-aspartate-evoked release of [H-3]dopamine in both striatal compartments. Altogether, these results suggest that substance P and eventually one of its metabolites, substance P(6-11) or another endogenous tachykinin released under the action of N-methyl-D-aspartate, contribute to the regulation of [H-3]dopamine release in both striatal compartments. They also extend previous observations which allowed us to demonstrate that the local circuits contributing to the presynaptic regulation of [H-3]dopamine release differ in striosome- and matrix-enriched areas. Furthermore, in agreement with observations made in some peripheral tissues, the present results support the existence of ''septide-sensitive'' tachykinin receptors in the rat striatum or alternatively of septide sensitive sites on tachykinin neurokinin-1 receptors distinct from those sensitive to neurokinin-1 receptor agonists, coupled to distinct transducing systems, and thus leading to biological responses which differ from those evoked by neurokinin-1 receptor agonists. Copyright (C) 1996 IBRO.