Activation of ionotropic GABA_A-depolarizes neurons that have high intracellular [Cl^-], causing inhibition or excitation in different cell types. The depolarization often leads to inactivation of voltage-gated Na-channels, but additional ionic mechanisms may also be affected. Previously, a simulated model of spider VS-3 mechanosensory neurons suggested that although voltage-activated Na⁺ current is partially inactivated during GABA induced depolarization, a slowly activating and inactivating component remains and may contribute to the depolarization. Here, we confirmed experimentally, by blocking Na-channels prior to GABA application, that Na⁺ current contributes to GABA induced depolarization in VS-3 neurons. Ratiometric Ca²⁺ imaging experiments combined with intracellular recordings revealed a significant increase in intracellular [Ca²⁺] when GABA_A-receptors were activated, synchronous with the depolarization and probably due to Ca²⁺ influx via low-voltage-activated (LVA) Ca-channels. In contrast, GABA_B-receptor activation in these neurons was previously shown to inhibit LVA current. Blockade of voltage-gated K-channels delayed membrane repolarization, extending GABA induced depolarization. However, inhibition of Ca-channels significantly increased the amplitude of GABA induced depolarization, indicating that Ca2⁺-activated K⁺ current has an even stronger repolarizing effect. Regulation of intracellular [Ca2+] is important for many cellular processes, and Ca²⁺ control of K⁺ currents may be particularly important for some functions of mechanosensory neurons, such as frequency tuning. These data show that GABA_A-receptor activation participates in this regulation.