Neuronal membrane properties can largely vary even within distinct morphological cell classes. The mechanisms and functional consequences of this diversity, however, are little explored. In the medial superior olive (MSO), a brainstem nucleus that performs binaural coincidence detection, membrane properties at rest are largely governed by the hyperpolarization-activated inward current (I-h) which enables the temporally precise integration of excitatory and inhibitory inputs. Here, we report that I-h density varies along the putative tonotopic axis of the MSO with I-h being largest in ventral, high-frequency (HF) processing neurons. Also I-h half-maximal activation voltage and time constant are differentially distributed such that I-h of the putative HF processing neurons activate faster and at more depolarized levels. Intracellular application of saturating concentrations of cyclic AMP removed the regional difference in hyperpolarization-activated cyclic nucleotide gated (HCN) channel activation, but not I-h density. Experimental data in conjunction with a computational model suggest that increased I-h levels are helpful in counteracting temporal summation of phase-locked inhibitory inputs which is particularly prominent in HF neurons.