Middle cerebral artery occlusions (MCAo) in rats produce infarcts in the pyriform and frontoparietal cortex, extending into the lateral basal ganglia and parasagittal cortex. We estimated tissue H2O concentrations from wet and dry weight measurements and determined Na and K concentrations by atomic absorption spectroscopy in these areas of rat brains. Tissue samples were analyzed at 2, 4, and 24 hours after MCAo and sham MCAo, compared with normal values measured in unoperated rats. In the pyriform and frontoparietal areas, H2O concentrations increased to 34 and 7% greater than normal by 2 hours, and 89 and 94% by 24 hours after MCAo. Na concentrations rose in these areas to 73 and 37% greater than normal by 2 hours, and 281 and 330% by 24 hours. K concentrations did not change until 4 hours, but fell to 62 and 34% of normal in these areas by 24 hours. Such large ion shifts indicate severe tissue destruction. In the parasagittal cortex and basal ganglia areas, the ion and water changes were smaller and did not become significant until 24 hours after MCAo. Rates of Na entry into the infarct site were greatest at 0-2 hours, while the rates of K loss peaked later, between 2 and 4 hours. The difference in Na influx and K efflux resulted in net ion shifts that correlated highly with water entry, yielding a correlation coefficient of 0.992 (p less than 0.001) and a slope indicating that 1 ml of water entered the tissue with each 145 mumoles of ions. These findings strongly suggest that net ion shifts cause the early edema of regional brain ischemia.(ABSTRACT TRUNCATED AT 250 WORDS)