Determination of compartment-specific cerebral blood volume (CBV) changes is important for understanding neurovascular physiology and quantifying blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI). In isoflurane-anesthetized cats, we measured the spatiotemporal responses of arterial CBV (CBV(a)) and total CBV (CBV(t)) induced by a 40-second visual stimulation, using magnetization transfer (MT)-varied BOLD and contrast-agent fMRI techniques at 9.4 T. To determine the venous CBV (CBV(v)) change, we calculated the difference between CBV(t) and CBV(a) changes. The dynamic response of CBV(a) was an order of magnitude faster than that of CBV(v), while the magnitude of change under steady-state conditions was similar between the two. Following stimulation offset, ΔCBV(a) showed small poststimulus undershoots, while ΔCBV(v) slowly returned to baseline. The largest CBV(a) and CBV(t) response occurred after 10 seconds of simulation in cortical layer 4, which we identified as the stripe of Gennari by T(1)-weighted MRI. The CBV(v) response, however, was not specific across the cortical layers during the entire stimulation period. Our data indicate that rapid, more-specific arterial vasodilation is followed by slow, less-specific venous dilation. Our finding implies that the contribution of CBV(v) changes to BOLD signals is significant for long, but not short, stimulation periods.