Top-down, auditory pallial regulation of the social behavior network

Abstract

Social encounters rely on sensory cues that carry nuanced information to guide social decision-making. While high-level features of social signals are processed in the telencephalic pallium, nuclei controlling social behaviors, called the social behavior network (SBN), reside mainly in the diencephalon. Although it is well known how mammalian olfactory pallium interfaces with the SBN, there is little information for how pallial processing of other sensory modalities can modulate SBN circuits. This is surprising given the importance of complex vocalizations, for example, for social behavior in many vertebrate taxa such as humans and birds. Using gregarious and highly vocal songbirds, female Zebra finches, we asked to what extent auditory pallial circuits provide consequential input to the SBN as it processes social sensory cues. We transiently inactivated auditory pallium of female Zebra finches during song playback and examined song-induced activation in SBN nuclei. Auditory pallial inactivation impaired responses to song specifically within the lateral ventromedial nucleus of the hypothalamus (VMHl), providing the first evidence in vertebrates of a connection between auditory pallium and the SBN. This same treatment elevated feeding behavior, which also correlated with VMHl activation. This suggests that signals from auditory pallium to VMHl can tune the balance between social attention and feeding drive. A descending influence of sensory pallium on hypothalamic circuits could therefore provide a functional connection for the integration of social stimuli with internal state to influence social decision-making. SignificanceSensory cues such as vocalizations contain important social information. These social signals can be substantially nuanced, containing information about vocalizer identity, prior experience, valence, and emotional state. Processing these features of vocalizations necessitates processing the fast, complex sound streams in song or speech, which depends on circuits in pallial cortex. But whether and how this information is then transferred to social circuits in limbic and hypothalamic regions remains a mystery. Here, we identify a top-down influence of the songbird auditory pallium on one specific node of the social behavior network within the hypothalamus. Descending functional connections such as these may be critical for the wide range of vertebrate species that rely on intricate sensory communication signals to guide social decision-making.