Abstract  Neuronal electrical oscillations in the theta (4–14 Hz) and gamma (30–80 Hz) ranges are necessary for performance of certain animal behaviors and cognitive processes. Perisomatic GABAergic inhibition is prominently involved in cortical oscillations driven by acetylcholine (ACh) release from septal cholinergic afferents. In neocortex and hippocampal CA3 regions, parvalbumin–positive (PV) basket cells, activated by ACh and glutamatergic agonists, largely mediate oscillations. However, in CA1 hippocampus in vitro, cholinergic agonists or optogenetic release of endogenous ACh from septal afferents induce rhythmic, theta‐frequency inhibitory post‐synaptic currents (IPSCs) in pyramidal cells, even with glutamatergic transmission blocked. The IPSCs are regulated by exogenous and endogenous cannabinoids, suggesting that they arise from type 1 cannabinoid‐receptor expressing (CB1R+) interneurons – mainly cholecystokinin (CCK) cells. Nevertheless, an occult contribution of PV interneurons to these rhythms remained conceivable. Here we directly test this hypothesis by selectively silencing CA1 PV cells optogenetically with halorhodopsin or archaerhodopsin. However, this had no effect on theta‐frequency IPSC rhythms induced by carbachol (CCh). In contrast, silencing glutamic‐acid‐decarboxylase 2+ interneurons, which include the CCK basket cells, strongly suppressed inhibitory oscillations; PV interneurons appear to play no role. The low‐frequency IPSC oscillations induced by CCh or optogenetically‐stimulated ACh release were also inhibited by a μ‐opioid receptor (MOR) agonist, which was unexpected because MORs in CA1 are not usually associated with CCK cells. Our results reveal novel properties of an inhibitory oscillator circuit within CA1 that is activated by muscarinic agonists. The oscillations could contribute to behaviourally‐relevant, atropine‐sensitive, theta‐rhythms and link cannabinoid and opioid actions functionally.