A comprehensive technique was developed for using three-dimensional (17)O magnetic resonance spectroscopic imaging at 9.4T for rapidly imaging the cerebral metabolic rate of oxygen consumption (CMRO(2)) in the rat brain during a two-min inhalation of (17)O(2). The CMRO(2) value (2.19 +/- 0.14 micromol/g/min, n = 7) was determined in the rat anesthetized with alpha-chloralose by independent and concurrent (17)O NMR measurements of cerebral H(2)17O content, arterial input function, and cerebral perfusion. CMRO(2) values obtained were consistent with the literature results for similar conditions. Our results reveal that, because of its superior sensitivity at ultra-high fields, the (17)O magnetic resonance spectroscopic imaging approach is capable of detecting small dynamic changes of metabolic H(2)17O during a short inhalation of (17)O(2) gas, and ultimately, for imaging CMRO(2) in the small rat brain. This study provides a crucial step toward the goal of developing a robust and noninvasive (17)O NMR approach for imaging CMRO(2) in animal and human brains that can be used for studying the central role of oxidative metabolism in brain function under normal and diseased conditions, as well as for understanding the mechanisms underlying functional MRI.