Knowledge of how vocal communication signals are represented in the auditory system is crucial for understanding the perceptual basis of vocal communication. Using male and female zebra finches, we identified a series of differentially expressed markers that helped define distinct (caudal, rostral, dorsal and ventral) domains within the caudomedial nidopallium (NCM), a high-order cortical auditory area known for its song-selective responses. Using expression analysis of the activity-inducible gene , we found that the number of activated neurons is more stimulus dependent in NCM than in the auditory midbrain or the caudomedial mesopallium, and that information on the density and spatial distribution of responsive neurons in NCM is sufficient to discriminate responses to conspecific song from other stimuli. We observed stronger activation of dorsal NCM, higher selectivity of caudal NCM towards conspecific song, and strong activation of the inhibitory network of rostral NCM by non-conspecific song stimuli. Song auditory representation in NCM was dependent on acoustic features, with the spatial organization of responsive cells particularly sensitive to both spectral and temporal components. We also obtained evidence of broadly distributed song-selective neuronal ensembles and that individual NCM neurons participate in the representation of conspecific songs, implying independent activation and molecular induction responses. We conclude that some basic aspects of the cortical response to complex auditory stimuli are topographically organized, a finding that has been elusive in other systems. These findings advance our knowledge of the functional organization of a key song-processing cortical area, providing novel insights into the auditory representation of conspecific vocal communication signals. Understanding how vocal signals are processed and represented in the brain is fundamental to the study of animal communication. Songbirds provide a powerful model for investigating these processes due to their rich vocal behavior and well-characterized neural circuits. Through analysis of differentially expressed markers and mapping of activity-induced gene expression, we have uncovered how different domains and neuronal populations within a high-order auditory cortical area respond to acoustic features of song and other stimuli. Besides providing in-depth knowledge of the functional organization of a key avian brain area, these findings provide insights into how acoustic features of complex learned vocal signals are processed and represented in cortical circuits, including evidence of how basic aspects of this representation can be topographically organized.