Sex differences in the representation of call stimuli in a songbird secondary auditory area

Nicolas Giret, Fabien Menardy, Catherine Del Negro

Understanding how communication sounds are encoded in the central auditory system is critical to deciphering the neural bases of acoustic communication. Songbirds use learned or unlearned vocalizations in a variety of social interactions. They have telencephalic auditory areas specialized for processing natural sounds and considered as playing a critical role in the discrimination of behaviorally relevant vocal sounds. The zebra finch, a highly social songbird species, forms lifelong pair bonds. Only male zebra finches sing. However, both sexes produce the distance call when placed in visual isolation. This call is sexually dimorphic, is learned only in males and provides support for individual recognition in both sexes. Here, we assessed whether auditory processing of distance calls differs between paired males and females by recording spiking activity in a secondary auditory area, the caudolateral mesopallium (CLM), while presenting the distance calls of a variety of individuals, including the bird itself, the mate, familiar and unfamiliar males and females. In males, the CLM is potentially involved in auditory feedback processing important for vocal learning. Based on both the analyses of spike rates and temporal aspects of discharges, our results clearly indicate that call-evoked responses of CLM neurons are sexually dimorphic, being stronger, lasting longer, and conveying more information about calls in males than in females. In addition, how auditory responses vary among call types differ between sexes. In females, response strength differs between familiar male and female calls. In males, temporal features of responses reveal a sensitivity to the bird's own call. These findings provide evidence that sexual dimorphism occurs in higher-order processing areas within the auditory system. They suggest a sexual dimorphism in the function of the CLM, contributing to transmit information about the self-generated calls in males and to storage of information about the bird's auditory experience in females.