Rhythmic firing is a common theme in cardiac and neuronal cells; where a rhythm is generated by intrinsic conductances, but regulated by extrinsic inputs. In the auditory brainstem, neurons of the superior paraolivary nucleus (SPN) exhibit rhythmic responses triggered by external sound stimulation. The SPN receives excitatory input from one ear, but action potential (AP) firing is suppressed by an inhibitory input during sound stimulation from the same ear. On release from this inhibition, SPN neurons respond with rebound APs generating a rhythmic offset-response. This signalling is considered to be important for detecting gaps and transients in sounds; a key feature for vocal communication. Here we use whole-cell patch recordings in mouse brainstem slices and sound-evoked single unit recordings in vivo to analyze the function of conductances that are activated near resting voltages and determine the ionic mechanism of this offset-response. For patch recordings CBA/CaJ mice (P14-P18) were killed by decapitation in accordance with the UK Animals (Scientific Procedures) Act 1986 and brainstem slices containing the superior olivary complex were prepared. The in vivo experiments were performed at the University of Washington, Seattle (USA) in accordance with the NIH Guide for the Care and Use of Laboratory. During the surgical preparation and recordings, the animals were anesthetized by intraperitoneal injection of a mixture of ketamine hydrochloride (100 mg/kg BW) and xylazine hydrochloride (5 mg/kg BW). A constant level of anesthesia was maintained throughout the recording experiments by hourly subcutaneaous injections of one-third of the initial dose. The spike firing and input-output functions of SPN neurons recorded under in vivo and in vitro conditions showed strong similarities. Injection of a hyperpolarizing current step under current-clamp in vitro showed the characteristic slow ‘sag’ of IH and a depolarizing offset-response, which triggered a burst of APs. Hyperpolarizing steps under voltage-clamp showed inward IH currents activating negative to -50mV. IH currents had a peak amplitude of 1.8 ±0.2nA (n=10) and were half-activated at -75.27 ±5.45mV (n=10). Block of IH currents by application of 20µM ZD7288 reduced and delayed, but did not eliminate offset-firing, suggesting multiple conductances were involved. SPN neurones also possessed a prominent T-type calcium current (ITCa) [ITCa: 0.8 ±0.2nA; time to peak-activation: 5.8 ±0.7ms; τdecay: 10.5 ±1.4ms; n=7] which was sensitive to mibefradil (2µM, n=3). Current clamp recordings confirmed that both IH and ITCa contribute to the generation of offset-responses. We conclude that during sound stimulation hyperpolarization caused by the synaptic IPSP, enhanced IH and reduced inactivation of ITCa so that on termination of the sound, the rapid repolarization triggers rebound AP firing through the cooperation of both conductances. Our results demonstrate that the temporal response of SPN neurons is not directly mediated via synaptic inputs, but requires the priming of intrinsic conductances by the IPSP, so that the observed rhythmic firing behaviour is an intricate combination of intrinsic and extrinsic signalling.