Motor-related forebrain areas in higher vertebrates also show responses to passively presented sensory stimuli. Sensory tuning properties in these areas, especially during wakefulness, and their relation to perception, however, are poorly understood. In the avian song system, HVC (proper name) is a vocal-motor structure with auditory responses well defined under anesthesia but poorly characterized during wakefulness. I used a large set of song stimuli including the bird‟s own song (BOS) and many conspecific stimuli (CON) to characterize auditory tuning properties in putative interneurons (HVCIN) during wakefulness. My findings suggest that HVC contains a heterogeneity of response types; a third of neurons are either suppressed or show no response to any stimuli and two thirds show excitatory responses to one or more stimuli. A subset of excitatory neurons are tuned exclusively to BOS and show very low linearity as measured by spectrotemporal receptive field analysis (STRF), but many respond well to both BOS and CON stimuli and show response linearity comparable to that previously measured in structures of the ascending auditory pathway. Fourier analysis of the STRFs of linear HVCIN reveals a range of peak spectrotemporal tuning properties, with approximately half of these neurons showing peak sensitivity to modulations occurring with high power in zebra finch song. Previous work has established that HVC lesioned birds are impaired in operant contingency reversals involving CON stimuli and birds with lesions to song nuclei receiving auditory input from HVC are impaired in discriminations between BOS and CON stimuli. The findings of the present study are consistent with these results and suggest a possible role for HVC in species-relevant auditory tasks.