The differentiated cytoarchitecture, neurochemistry, and capillary organization of the rat dorsal vagal complex prompted this comprehensive investigation of microvascular physiology in 11 subdivisions of area postrema, 5 subnuclei of nucleus tractus solitarii (NTS), the dorsal motor nucleus of the vagus nerve, and 4 other gray matter structures in the dorsal medulla oblongata. Microvascular exchangeable volume (residual plasma volume), capillary blood and plasma flow, and unidirectional transfer constants for a tracer amino acid, [C-14]alpha-aminoisobutyric acid (AIB), varied considerably among the structures analyzed. Exchangeable volume, largest in area postrema medial zones (about 29-mu-l.g-1) and smallest in medullary gray matter (7-11-mu-l.g-1), correlated directly with subregional densities of capillaries and rates of tissue glucose metabolism. Capillary blood flow (range of 1,430-2,147-mu-l.g-1.min-1), plasma flow, and tissue glucose metabolism (range of 0.48-0.71-mu-mol.g-1.min-1) were linearly related in the dorsal vagal complex. The most striking quantitative difference among structures in this brain region were the rates of transcapillary influx and derived permeability x surface area (PS) products of [C-14]AIB, which has physicochemical properties resembling those of hormones. PS products for AIB were negligible in most medullary gray matter regions (< 1-mu-l.g-1.min-1, indicative of blood-brain barrier properties), but were 20-59 x and 99-402 x higher in NTS subnuclei and area postrema, respectively. An extraordinary feature of the microcirculation in area postrema was the long-duration transit of tracer sucrose and blood, a characteristic that would amplify the sensing ability of area postrema as it monitors the composition of the circulation.