Despite the different origins of cerebrovascular activity induced by neurogenic and nonneurogenic conditions, a standard assumption in functional studies is that the consequence on the vascular system will be mechanically similar. Using a recently developed arterial spin labeling method, we examined arterial blood volume, arterial-microvascular transit time, and cerebral blood flow (CBF) in the gray matter and in areas with large arterial vessels under hypercapnia, visual stimulation, and a combination of the two. Spatial heterogeneity in arterial reactivity was observed between conditions. During hypercapnia, large arterial volume changes contributed to CBF increase and further downstream, there were reductions in the gray matter transit time. These changes were not significant during visual stimulation, and during the combined condition they were moderated. These findings suggest distinct vascular mechanisms for large and small arterial segments that may be condition specific. However, the power relationships between gray matter arterial blood volume and CBF in hypercapnia (α = 0.69 ± 0.24) and visual stimulation (α = 0.68 ± 0.20) were similar. Assuming consistent capillary and venous volume responses across these conditions, these results offer support for a consistent total CBV–flow relationship typically assumed in blood oxygen-level dependent calibration techniques.