Octopus cells, neurons in the most posterior and dorsal part of the mammalian ventral cochlear nucleus, convey the timing of synchronous firing of auditory nerve fibers to targets in the contralateral superior paraolivary nucleus and ventral nucleus of the lateral lemniscus. The low input resistances and short time constants at rest that arise from the partial activation of a large, low-voltage-activated K+ conductance (gKL) and a large mixed-cation, hyperpolarization-activated conductance (gh) enable octopus cells to detect coincident firing of auditory nerve fibers with exceptional temporal precision. Octopus cells fire conventional, Na+ action potentials but a voltage-sensitive Ca2+ conductance was also detected. In this study, we explore the nature of that calcium conductance under voltage-clamp. Currents, carried by Ca2+ or Ba2+ and blocked by 0.4 mM Cd2+, were activated by depolarizations positive to −50 mV and peaked at −23 mV. At −23 mV they reached 1.1 ± 0.1 nA in the presence of 5 mM Ca2+ and 1.6 ± 0.1 nA in 5 mM Ba2+. Ten micromolar BAY K 8644, an agonist of high-voltage-activated L-type channels, enhanced IBa by 63 ± 11% (n = 8) and 150 μM nifedipine, an antagonist of L-type channels, reduced the IBa by 65 ± 5% (n = 5). Meanwhile, 0.5 μM ω-Agatoxin IVA, an antagonist of P/Q-type channels, or 1 μM ω-conotoxin GVIA, an antagonist of N-type channels, suppressed IBa by 15 ± 4% (n = 5) and 9 ± 4% (n = 5), respectively. On average 16% of the current remained in the presence of the cocktail of blockers, indicative of the presence of R-type channels. Together these experiments show that octopus cells have a depolarization-sensitive gCa that is largely formed from L-type Ca2+ channels and that P/Q-, N-, and R-type channels are expressed at lower levels in octopus cells.