The Forebrain Song System Mediates Predictive Call Timing in Female and Male Zebra Finches

The dichotomy between vocal learners and non-learners is a fundamental distinction in the study of animal communication. Male zebra finches (Taeniopygia guttata) are vocal learners that acquire a song resembling their tutors’, whereas females can only produce innate calls. The acoustic structure of short calls, produced by both males and females, is not learned. However, these calls can be precisely coordinated across individuals. To examine how birds learn to synchronize their calls, we developed a vocal robot that exchanges calls with a partner bird. Because birds answer the robot with stereotyped latencies, we could program it to disrupt each bird’s responses by producing calls that are likely to coincide with the bird’s. Within minutes, the birds learned to avoid this disruptive masking (jamming) by adjusting the timing of their responses. Notably, females exhibited greater adaptive timing plasticity than males. Further, when challenged with complex rhythms containing jamming elements, birds dynamically adjusted the timing of their calls in anticipation of jamming. Blocking the song system cortical output dramatically reduced the precision of birds’ response timing and abolished their ability to avoid jamming. Surprisingly, we observed this effect in both males and females, indicating that the female song system is functional rather than vestigial. We suggest that descending forebrain projections, including the song-production pathway, function as a general-purpose sensorimotor communication system. In the case of calls, it enables plasticity in vocal timing to facilitate social interactions, whereas in the case of songs, plasticity extends to developmental changes in vocal structure. •Zebra finches can learn to modify the timing of their innate calls•Birds dynamically adjust call timing in anticipation of complex rhythm patterns•Non-singing females exhibit strong call timing plasticity•The song control system is necessary for predictive call timing and precision Benichov et al. show that zebra finches predictively adjust the timing of unlearned calls in response to rhythmic call patterns. Female zebra finches, who don’t sing, show better call timing plasticity than males. In both sexes, the forebrain song system is required for this learning, suggesting a role for this circuit in interactive vocal coordination.