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As arteries are resistance blood vessels while veins perform a capacitance function, it might be expected that sympathetic neural control of arteries and veins would differ. The function of sympathetic nerves supplying mesenteric arteries (MA) and veins (MV) in rats was investigated using in vitro continuous amperometry with a carbon fibre microelectrode and video imaging. We simultaneously measured noradrenaline (NA) overflow at the blood vessel adventitial surface and vasoconstriction evoked by electrical stimulation of perivascular sympathetic nerves. Sympathetic nerve arrangement was studied using glyoxylic acid-induced fluorescence of NA. We found that: (i) there were significant differences between MA and MV in the arrangement of sympathetic nerves; (ii) frequency–response curves for NA overflow and vasoconstriction for MV were left-shifted compared to MA; (iii) the P2X receptor antagonist, pyridoxal-phosphate-6-azophenyl-2′,4′-disulphonic acid (PPADS, 10 μm), reduced constrictions in MA but not in MV while the α1-adrenergic receptor antagonist, prazosin (0.1 μm), blocked constrictions in MV but not in MA; (iv) NA overflow for MA was enhanced by the α2-adrenergic receptor antagonist, yohimbine (1.0 μm), and attenuated by the α2-adrenergic receptor agonist, UK 14,304 (1.0 μm), while yohimbine and UK 14,304 had little effect in MV; (v) cocaine (10 μm) produced larger increases in NA overflow in MA than in MV; (vi) UK 14,304 constricted MV but not MA while yohimbine reduced constrictions in MV but not MA. We conclude that there are fundamental differences in sympathetic neuroeffector mechanisms in MA and MV, which are likely to contribute to their different haemodynamic functions.