We investigated the role of trabecular smooth muscle tone in regulation of intracavernosal pressure, venous outflow resistance, and penile capacitance. In an isolated rabbit whole penis model, corpora cavernosa were infused with either contracting (high K(+)-norepinephrine combination) or relaxing (no added Ca(2+)-papaverine combination) physiological salt solutions while intracavernosal pressure was recorded. An infusion pump regulated by an intracavernosal pressure feedback mechanism enabled the measurement of flow necessary to maintain intracavernosal pressures at 30, 60, 90, 120, and 150 mmHg under steady-state conditions (inflow = outflow). These experiments allowed resistance to outflow from corpora to be calculated when trabecular smooth muscle was either constricted or relaxed. Decay in intracavernosal pressure over time from various predetermined intracavernosal pressures (150, 120, 90, 60, and 30 mmHg) was studied under conditions of zero inflow following contraction or relaxation of trabecular smooth muscle. This permitted calculation of the time constant, which together with the outflow resistance, permitted the calculation of penile capacitance. When smooth muscle is relaxed, venous outflow resistance is high, constant, and independent of intracavernosal pressure. Furthermore, relaxation of smooth muscle allows expansion of corpora with accumulation of volume under pressure, enabling the penis to act as a capacitor. This capacitor function is limited in the presence of constant high outflow resistance by stiffness of the fibroelastic elements of penis, tunica, and fibroelastic frame, which exhibit nonlinear deflection trends. Analysis of these variables has led us to propose a model for penile erection.