In functional magnetic resonance imaging (fMRI), neural activity is inferred from the associated hemodynamic response. However, the degree to which hemodynamics can track dynamic changes in neuronal activity, and thus the ultimate temporal resolution of fMRI, remains unknown. To evaluate the detectability of stimulus-driven high-frequency blood oxygenation level dependent (BOLD) signal oscillations in functionally and vascularly distinct cerebral cortical areas, stimuli up to 0.5 Hz were used to evoke activation in the primary somatosensory and motor cortex. Despite their functional and vascular differences, a similar frequency dependence was observed in both cortical areas. We then proceeded to investigate these signals at different levels of the cortical vascular hierarchy, using cortical depth as a proxy. We observed that, above 0.33 Hz, the BOLD response amplitude decreased faster with increasing frequency near the pial surface than in the parenchyma, suggesting that, in addition to exhibiting high spatial specificity, parenchymal signals—accessible with high spatial resolution imaging—also attenuate less rapidly when the stimulus frequency is increased. In addition, as the stimulus frequency increased, we observed larger relative phase differences in the BOLD oscillations across cortical depths. When averaged across depths, these signals can thus interfere destructively, suggesting that high spatial resolutions can avoid this phase cancellation and thereby aid in the detection of rapid BOLD oscillations.