Physiological and morphometric studies were conducted on the microvascular endothelium of four individual cerebral structures having different neural activities--the inferior colliculus, sensorimotor cortex (both gray matter regions), genu of the corpus callosum (white matter), and the subfornical organ (a circumventricular organ) of rats. The physiological data, obtained by quantitative autoradiography, produced new findings: the rate of blood-to-tissue flux across capillary endothelial cells of a neutral amino acid, 14C-alpha-aminoisobutyric acid, was 100-400 X more rapid in the subfornical organ than in gray and white matter regions, and the transit time of labeled albumin in the subfornical organ microcirculation was 7-12 X longer than in the blood-brain barrier regions. These quantitative studies suggest that circulating messengers, such as hormones, would have more prolonged receptor contact with capillary endothelial cells and greater rates of transendothelial passage in the subfornical organ than in gray or white matter. Capillary densities, volume fractions, and surface areas were similar for the inferior colliculus (which has the highest rates of tissue glucose metabolism and blood flow among blood-brain barrier regions) and the subfornical organ, but were significantly smaller for sensorimotor cortex and corpus callosum (about 35 and 70% lower, respectively). Electron microscopic morphometry of capillary endothelial cells in the inferior colliculus and corpus callosum indicated the ultrastructural basis of blood-brain barrier mechanisms in these regions--intercellular junctions that appeared tight, few cytoplasmic vesicular profiles, and no fenestrations. Analysis of endothelial cells in the subfornical organ demonstrated 7 X more vesicular profiles and 4 fenestrations per cross section of capillary. These findings represent structural evidence for high rates of solute flux across the capillary endothelium of circumventricular organs.