Cranial parasympathetic activation produces vasodilation in the head and neck region, but little is known about its central and peripheral mechanisms. This study was conducted to examine whether external and internal carotid-vasodilation origin sites triggered by chemical stimulation are distributed topographically in the parasympathetic brainstems of anesthetized rats, and to examine the effects of peripheral receptors on vasodilation. Microinjection of the neuromodulator candidate l -cysteine revealed that external and internal carotid vasodilation–triggering sites were distributed non-topographically along the full extent of the parasympathetic parvocellular reticular formation (PcRt). Intravenous injection of a muscarinic blocker and a nitric oxide synthase inhibitor abolished external carotid vasodilation, suggesting the peripheral involvement of muscarinic and nitric oxide receptors. Further work is needed to fully understand the PcRt mechanisms underlying timely and appropriate vasodilation to support various cranial functions.