Duets recorded in the wild reveal that interindividually coordinated motor control enables cooperative behavior

Susanne Hoffmann,Andries Ter Maat,Alena Lemazina,Markus Abels,Lisa Trost,Manfred Gahr,Hannes Sagunsky,Sandra Kollmansperger,Cornelia Voigt,Stefan Leitner

doi:10.1038/s41467-019-10593-3

Abstract

Many organisms coordinate rhythmic motor actions with those of a partner to generate cooperative social behavior such as duet singing. The neural mechanisms that enable rhythmic interindividual coordination of motor actions are unknown. Here we investigate the neural basis of vocal duetting behavior by using an approach that enables simultaneous recordings of individual vocalizations and multiunit vocal premotor activity in songbird pairs ranging freely in their natural habitat. We find that in the duet-initiating bird, the onset of the partner’s contribution to the duet triggers a change in rhythm in the periodic neural discharges that are exclusively locked to the initiating bird’s own vocalizations. The resulting interindividually synchronized neural activity pattern elicits vocalizations that perfectly alternate between partners in the ongoing song. We suggest that rhythmic cooperative behavior requires exact interindividual coordination of premotor neural activity, which might be achieved by integration of sensory information originating from the interacting partner.

Highlights

Many organisms coordinate rhythmic motor actions with those of a partner to generate cooperative social behavior such as duet singing
We analyzed 647 duet bouts produced by eight P. mahali pairs
In accordance with previous work[12], we found that duet bouts of P. mahali generally consisted of syllables sung by a single bird to initiate duetting, followed by male and female syllables that built the actual duet

Summary

Introduction

Many organisms coordinate rhythmic motor actions with those of a partner to generate cooperative social behavior such as duet singing. We suggest that rhythmic cooperative behavior requires exact interindividual coordination of premotor neural activity, which might be achieved by integration of sensory information originating from the interacting partner. While in some bird species vocalizations from both duet partners temporally overlap to a variable degree[2,3,4], other birds produce vocal duets in which the partners’ contributions alternate almost perfectly[5,6,7]. The temporal dynamics of male and female vocal productions during duetting are, unknown Another large gap in knowledge exists regarding the neural mechanisms mediating the precise interindividual coordination of vocalizations during duetting[13]. HVC neurons show selective responses to auditory presentations of the bird’s own vocalizations[22,23,24]

Methods

Results

Conclusion