Exaggerated arginine vasopressin (AVP) induced calcium signaling and renal vasoconstriction, characteristic in young spontaneously hypertensive rats (SHR) during euvolemia, are related to greater amounts of V_1a receptor mRNA and V_1a protein in preglomerular resistance arterioles. The present study determined whether V_1a receptor density and calcium signal transduction in the renal vasculature of young SHR is regulated appropriately during physiological changes in hydration state. [³H]AVP ligand binding documented 2-3 fold greater density of V_1a receptors in euvolemic SHR vs. Wistar Kyoto rats (WKY). Parallel changes in V_1a receptor density were observed in both strains during chronic water loading (+ ~ 50 fmol/mg) and during dehydration ( - ~ 50 fmol/mg). Affinity was unchanged. Real-time RT-PCR demonstrated that V_1a mRNA in preglomerular arterioles was 3 times greater in euvolemic SHR. Dehydration decreased expression about 50% in renal vessels independent of rat strain; water loading increased V_1a mRNA. Thus, V_1a receptor regulation correlated with changes in mRNA in a normal manner in response to chronic changes in AVP concentration, albeit set at a higher level in SHR. In dehydrated animals, AVP increased the cytosolic Ca²⁺ concentration [Ca²⁺ ]_i by 60 ± 5 nM Ca²⁺ _i and 112 ± 13 nM Ca²⁺ _i in WKY and SHR, respectively (p < 0.01), while in hydrated animals the [Ca²⁺ ]_i increase was 168 ± 10 nM and 220 ± 18, respectively (p < 0.05). In all hydration states, calcium signaling was greater in SHR compared to WKY (p < 0.05). Calcium signaling paralleled changes in the receptor density and mRNA. Mechanisms other than hydration state per se are likely to be responsible for the 2-3 fold difference in the V1a receptor density between WKY and SHR in the renal vasculature at the critical age of 6 weeks.