The presence of an audience modulates responses to familiar call stimuli in the male zebra finch forebrain.

The ability to recognize familiar individuals is crucial for establishing social relationships. The zebra finch, a highly social songbird species that forms lifelong pair bonds, uses a vocalization, the distance call, to identify its mate. However, in males, this ability depends on social conditions, requiring the presence of an audience. To evaluate whether the presence of bystanders modulates the auditory processing underlying recognition abilities, we assessed, by using a lightweight telemetry system, whether electrophysiological responses driven by familiar and unfamiliar female calls in a high-level auditory area [the caudomedial nidopallium (NCM)] were modulated by the presence of conspecific males. Males had experienced the call of their mate for several months and the call of a familiar female for several days. When they were exposed to female calls in the presence of two male conspecifics, NCM neurons showed greater responses to the playback of familiar female calls, including the mate's call, than to unfamiliar ones. In contrast, no such discrimination was observed in males when they were alone or when call-evoked responses were collected under anaesthesia. Together, these results suggest that NCM neuronal activity is profoundly influenced by social conditions, providing new evidence that the properties of NCM neurons are not simply determined by the acoustic structure of auditory stimuli. They also show that neurons in the NCM form part of a network that can be shaped by experience and that probably plays an important role in the emergence of communication sound recognition.

Social experience affects neuronal responses to male calls in adult female zebra finches.

Plasticity studies have consistently shown that behavioural relevance can change the neural representation of sounds in the auditory system, but what occurs in the context of natural acoustic communication where significance could be acquired through social interaction remains to be explored. The zebra finch, a highly social songbird species that forms lifelong pair bonds and uses a vocalization, the distance call, to identify its mate, offers an opportunity to address this issue. Here, we recorded spiking activity in females while presenting distance calls that differed in their degree of familiarity: calls produced by the mate, by a familiar male, or by an unfamiliar male. We focused on the caudomedial nidopallium (NCM), a secondary auditory forebrain region. Both the mate's call and the familiar call evoked responses that differed in magnitude from responses to the unfamiliar call. This distinction between responses was seen both in single unit recordings from anesthetized females and in multiunit recordings from awake freely moving females. In contrast, control females that had not heard them previously displayed responses of similar magnitudes to all three calls. In addition, more cells showed highly selective responses in mated than in control females, suggesting that experience-dependent plasticity in call-evoked responses resulted in enhanced discrimination of auditory stimuli. Our results as a whole demonstrate major changes in the representation of natural vocalizations in the NCM within the context of individual recognition. The functional properties of NCM neurons may thus change continuously to adapt to the social environment.