We used auditory responsiveness in the avian song system to investigate the complex relationship between behavioral state and sensory processing in a high-order sensorimotor brain area. We present evidence from recordings in awake, anesthetized, and sleeping male zebra finches (Taeniopygia guttata) that auditory responsiveness in nucleus HVc is profoundly affected by changes in behavioral state. In anesthetized and sleeping birds, auditory responses were characterized by an increase in firing rate that was selective for the bird's own song (BOS) and highly stable over time. In contrast, HVc responses during wakefulness were extremely variable and transitioned between undetectable and robust levels over short intervals. Surprisingly, auditory responses in awake birds were not selective for the BOS stimulus. The variability of HVc auditory responses in awake birds suggests that, as in mammals, wakefulness is not a uniform behavioral state. Rather, auditory responsiveness likely is continually influenced by variables such as arousal state. We therefore developed several experimental paradigms in which we could manipulate arousal levels during auditory stimulus presentation. In all cases, arousal suppressed HVc auditory responses. This effect was specific to the song system, as auditory responses in Field L, a primary auditory area that is a source of auditory input to HVc, were unaffected. While arousal acts as a negative regulator of HVc auditory responsiveness, the presence and variability of the responses observed in awake, alert birds suggests that other mechanisms, such as attention, may enhance auditory responsiveness. The interplay between behavioral state and sensory processing may regulate song system responsiveness according to the bird's behavioral and social context.