Neurophysiological coordination of duet singing
Significance Cooperation, turn taking, and other social behaviors often depend on temporal coordination between individuals. How brains use sensory cues from participants to synchronize performances is not known. We examined the interactions between sensory cues and motor activity in the brains of female and male plain-tailed wrens that rapidly take turns to produce a duet that sounds as if a single bird is singing. We made simultaneous neurophysiological recordings from the brains of pairs of awake, duetting wrens. We discovered that inhibition driven by auditory feedback from the partner alternated with the premotor activity used by each individual to produce its own vocalizations. These data show how sensory feedback links the brains of cooperating animals through the modulation of motor circuits. Coordination of behavior for cooperative performances often relies on linkages mediated by sensory cues exchanged between participants. How neurophysiological responses to sensory information affect motor programs to coordinate behavior between individuals is not known. We investigated how plain-tailed wrens (Pheugopedius euophrys) use acoustic feedback to coordinate extraordinary duet performances in which females and males rapidly take turns singing. We made simultaneous neurophysiological recordings in a song control area “HVC” in pairs of singing wrens at a field site in Ecuador. HVC is a premotor area that integrates auditory feedback and is necessary for song production. We found that spiking activity of HVC neurons in each sex increased for production of its own syllables. In contrast, hearing sensory feedback produced by the bird’s partner decreased HVC activity during duet singing, potentially coordinating HVC premotor activity in each bird through inhibition. When birds sang alone, HVC neurons in females but not males were inhibited by hearing the partner bird. When birds were anesthetized with urethane, which antagonizes GABAergic (γ-aminobutyric acid) transmission, HVC neurons were excited rather than inhibited, suggesting a role for GABA in the coordination of duet singing. These data suggest that HVC integrates information across partners during duets and that rapid turn taking may be mediated, in part, by inhibition.