The insect mushroom bodies (MBs) are multimodal signal processing centers and essential for olfactory learning. Electrophysiological recordings from the MBs' principal component neurons, the Kenyon cells (KCs), showed a sparse representation of olfactory signals. It has been proposed that the intrinsic and synaptic properties of the KC circuitry combine to reduce the firing of action potentials and to generate relatively brief windows for synaptic integration in the KCs, thus causing them to operate as coincidence detectors. To better understand the ionic mechanisms that mediate the KC intrinsic firing properties, we used whole-cell patch-clamp recordings from KCs in the adult, intact brain of Periplaneta americana to analyze voltage- and/or Ca²⁺- dependent inward (I_Ca, I_Na) and outward currents (I_A, I_K(V), I_K,ST, I_O(Ca)). In general the currents had properties similar to currents in other insect neurons. Certain functional parameters of I_Ca and I_O(Ca), however, had extreme values allowing them to assist sparse coding. I_Ca had a low activation threshold and a very high current density compared to I_Ca in other insect neurons. Together these parameters make I_Ca suitable for boosting and sharpening the EPSPs as reported in previous studies. I_O(Ca) also had a large current density and a very depolarized activation threshold. In combination, the large I_Ca and I_O(Ca) are likely to mediate the strong spike frequency adaptation. These intrinsic properties of the KCs are likely to be supported by their tonic, inhibitory synaptic input, which was revealed by specific GABA antagonists, and which contributes significantly to the hyperpolarized membrane potential at rest.