The nucleus accumbens (NAc) is a forebrain area in the mesocorticolimbic dopamine (DA) system that regulates many aspects of drug addiction. Neuronal activity in the NAc is modulated by different subtypes of DA receptors. Although DA signaling has received considerable attention, the mechanisms underlying D₂-class receptor (D₂R) modulation of firing in medium spiny neurons (MSNs) localized within the NAc remain ambiguous. In the present study, we performed whole-cell current-clamp recordings in rat brain slices to determine whether and how D₂R modulation of K⁺ channel activity regulates the intrinsic excitability of NAc neurons in the core region. D₂R stimulation by quinpirole or DA significantly and dose-dependently decreased evoked Na⁺ spikes. This D₂R effect on inhibiting evoked firing was abolished by antagonism of D₂Rs, reversed by blockade of voltage-sensitive, slowly-inactivating A-type K⁺ currents (I_As), or eliminated by holding membrane potentials at levels in which I_As was inactivated. It was also mimicked by inhibition of cAMP-dependent protein kinase (PKA) activity, but not phosphatidylinositol-specific phospholipase C (PI-PLC) activity. Moreover, D₂R stimulation also reduced the inward rectification and depolarized the resting membrane potentials (RMP) by decreasing "leak" K⁺ currents. However, the D₂R effects on inward rectification and RMP were blocked by inhibition of PI-PLC, but not PKA activity. These findings indicate that, with facilitated intracellular Ca²⁺ release and activation of the D₂R/Gq/PLC/PIP₂ pathway, the D₂R-modulated changes in the NAc excitability are dynamically regulated and integrated by multiple K⁺ currents, including but are not limited to I_As, inwardly rectifying K⁺ currents (I_Kir), and "leak" currents (I_K-2P).