Activity of the magnocellular neurons that synthesize vasopressin in the supraoptic and paraventricular nuclei of the hypothalamus is modulated by local release of the neuropeptide within the nuclei. V(1a) and V(1b) vasopressin receptor genes are expressed in these cells. The present study reports the localization of V(1a) and V(1b) receptors using multiple labeling immunocytochemistry. Both receptors are mainly located in vasopressinergic magnocellular neurons and colocalized with vasopressin in cytoplasmic vesicles dispersed throughout the cell. Possible functional modifications of the mRNA and protein levels of the V(1a) receptor, the major isoform, were also investigated by semiquantitative in situ hybridization and immunocytochemistry in rats submitted to reduced or increased water intake. V(1a) mRNA and receptor levels varied with water balance. V(1a) mRNA level dropped in rats submitted to high water intake. Conversely, dehydration up-regulated the V(1a) receptor content. These observations suggest that the pathways that regulate the expression of the genes encoding vasopressin and the V(1a) receptor are linked, which fits the present findings that the two partners are colocalized in cytoplasmic vesicles. Colocalization might explain how V(1) autoreceptors are controlled by cell activity and/or local concentration of vasopressin (released locally by the neurons themselves), allowing fine adjustment of magnocellular neuron activity.