The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA_A-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on NCM, an area analogous to parts of the mammalian auditory cortex, with selective responses to birdsong. We present evidence that GABA_A-mediated inhibition plays a pronounced role in NCMs auditory processing of birdsong. Using immunocytochemistry we show that approximately half of NCMs neurons are GABAergic. Whole-cell patch-clamp recordings in a slice preparation demonstrate that, at rest, spontaneously active GABAergic synapses inhibit excitatory inputs onto NCM neurons via GABA_A receptors. Multi-electrode electrophysiological recordings in awake birds show that local blockade of GABA_A-mediated inhibition in NCM markedly affects the temporal pattern of song-evoked responses in NCM without modifications in frequency tuning. Surprisingly, this blockade increases the phasic and largely suppresses the tonic response component, reflecting dynamic relationships of inhibitory networks that could include disinhibition. Thus, processing of learned natural communication sounds in songbirds, and possibly other vocal learners, may depend on complex interactions of inhibitory networks.