Spectral analysis of cardiovascular signals has been extensively used to investigate circulatory homeostatic mechanisms. However, the nature of very low-frequency (VLF) fluctuations is still unclear. Because we previously observed enhanced VLF fluctuations of blood pressure (BP) in the sympathectomized rat (a model characterized by markedly increased plasma epinephrine levels), aims of our study were to assess whether the genesis of VLF BP fluctuations depends on circulating catecholamines and which adrenergic receptor(s) as well as which membrane ion channel(s) are involved. Using continuous intraarterial BP recordings from unanesthetized unrestrained rats, VLF BP power was computed in the intact condition, during acute ganglionic blockade with hexamethonium and after restoration of BP levels by infusion (on top of hexamethonium) of adrenergic agonists (epinephrine, norepinephrine, clonidine) or non adrenergic vasoconstrictors (vasopressin). Moreover, the effects on VLF BP fluctuations of specific adrenergic receptor blockers (propranolol, prazosin, yohimbine) infused on top of hexamethonium plus catecholamines were assessed. Finally, the effects of various membrane ion channel blockers were also evaluated. Results: i) ganglionic blockade drastically reduced BP levels and VLF fluctuations; ii) all vasoconstrictors restored BP levels but only the adrenergic ones generated striking VLF BP fluctuations; iii) catecholamine-induced fluctuations were abolished by alpha-2 (but not alpha-1 or beta) adrenergic receptor blockade, and by barium sensitive K⁺-channel or L-type Ca⁺⁺-channel but not by other ion channel blockers. Conclusions: in the conscious, unrestrained ganglion-blocked rat, catecholamine infusion generates VLF BP fluctuations through stimulation of alpha-2 receptors and activation of barium sensitive K⁺ channels. These fluctuations may have (patho)physiological relevance under conditions of disrupted circulatory homeostasis.