The ultimate goal of high-resolution functional brain mapping is single-condition (stimulus versus no-stimulus maps) rather than differential imaging (comparing two “stimulus maps”), because the appropriate (“orthogonal”) stimuli are rarely available. This requires some component(s) of activity-dependent hemodynamic signals to closely colocalize with electrical activity, like the early increase in deoxyhemoglobin, shown previously to yield high-quality functional single-condition maps. Conversely, nonlocal vascular responses dominate in cerebral blood volume (CBV)-based single-condition maps. Differential CBV maps are largely restricted to the parenchyma, implying that part of the CBV response does colocalize with electrical activity at fine spatial scale. By removing surface vascular activation from optical imaging data, we document the existence of a capillary CBV response component, regulated at fine spatial scale and yielding single-condition maps exhibiting ∼100 μm resolution. Blood volume and -flow based single-condition functional mapping at columnar level should thus be feasible, provided that the capillary response component is selectively imaged.