Passive Physiological Responses Fail to Predict Context-Dependent Action Selection in Bats

Abstract

How social animals encode vocalizations, assign them value, and formulate behavioral responses remains largely unknown. We asked whether physiological signatures of social-call perception predict behavioral responses across contexts, using the Egyptian Fruit Bat (Rousettus aegyptiacus), an auditory specialist with a rich repertoire of social calls. Using heart rate monitoring during playback of conspecific vocalizations, we found that females showed larger heart rate responses than males to social calls (aggression and distress), whereas non-social echolocation calls evoked no sex difference. In vivo recordings from primary auditory cortex (A1) revealed call-selective units whose selectivity was independent of frequency tuning, with the largest selective fraction for distress calls. In a behavioral assay, female bats approached a distress-call playback only when a live conspecific was coupled with it. However, in isolation, the same calls elicited interest (grooming, pointing) but no approach. Together, the neural and autonomic signatures of social-call perception are present across contexts, whereas the behavioral response is not. Social context, therefore, does not modulate the behavioral readout of social calls; rather, it gates it. Significance StatementHow a social animal converts the perception of a vocalization into behavior remains poorly understood. Using the Egyptian Fruit Bat (Rousettus aegyptiacus), we show that physiological and neural responses to social calls are present in isolation, whereas approach behavior is not. We conclude that social context acts as a necessary gate between sensory representation and action, not a modulator that adjusts an existing response.