Spontaneous purinergic neurotransmission was characterised in the mouse urinary bladder. Intracellular electrophysiological recording from smooth muscle cells of the detrusor muscle revealed spontaneous depolarizations, distinguishable from spontaneous action potentials (sAPs) by their amplitude (<40 mV) and insensitivity to the L-type Ca²⁺ channel blocker nifedipine (1 μM) (mean ± S.E.M., 100 ± 29%; Student’s two-tailed paired t-test, P = NS, n = 4). Spontaneous depolarizations were abolished by the P2X₁ receptor antagonist NF449 (10 μM) (frequency 8.5 ± 8.5% of controls, P < 0.01), insensitive to the muscarinic acetylcholine receptor antagonist atropine (1 μM) (103.4 ± 3.0%, P = NS), and became more frequent in latrotoxin (1 nM) (438 ± 95%, P < 0.05), suggesting that they are spontaneous excitatory junction potentials (sEJPs). Such sEJPs were correlated, in amplitude and timing, with focal Ca²⁺ transients in smooth muscle cells (measured using confocal microscopy), suggesting a common origin: ATP binding to P2X₁ receptors. sAPs were also abolished by NF449, insensitive to atropine (126 ± 39%, P = NS) and increased in frequency by LTX (930 ± 450%, P < 0.05) suggesting a neurogenic, purinergic origin, in common with sEJPs. By comparing the kinetics of sAPs and sEJPs, we demonstrated that sAPs occur when sufficient cation influx through P2X₁ receptors triggers L-type Ca²⁺ channels; the first peak of the differentiated rising phase of depolarizations – attributed to the influx of cations through the P2X₁ receptor – is of larger median amplitude for sAPs (2248 mV.s^-1) than sEJPs (439 mV.s^-1; Wilcoxon signed rank test, P < 0.0001). Surprisingly, sAPs in the mouse urinary bladder are triggered by stochastic ATP release from parasympathetic nerve terminals rather than being myogenic.