A fundamental feature of vocal communication is taking turns: when one person says something, the other person listens and then responds. Turn-taking requires precise coordination of the timing of signals between individuals. We have all found over the past year communicating over Zoom that disruptions of the timing of auditory cues—like those annoying delays caused by poor connections—make effective communication difficult and frustrating. How do the brains of two individuals synchronize their activity patterns for rapid turn-taking during vocal communication?
We addressed this question in a recently published paper by studying turn-taking in a specialist, the plain-tailed wren (Pheugopedius euophrys), which sings precisely timed duets. Our findings demonstrate the ability to coordinate relies on sensory cues from one partner that temporarily inhibit vocalizations in the other.
These birds sing duets in which females and males alternate their vocalizations, called syllables, so rapidly it sounds as if a single bird is singing. These wrens live in dense bamboo on the slopes of the Andes. To study the neural basis of duet singing, we flew to Ecuador where we loaded up a truck with equipment and drove to a remote field-site called the Yanayacu Biological Field Station and Center for Creative Studies. Much of our equipment required electricity, so we had to bring car batteries for backup and used a six-meter copper rod that we drove into the soft mountain earth for our electrical ground. Our “lab bench” was a door that we placed on two Pelican suitcases.
First, we had to catch pairs of wrens, so we hacked through bamboo with machetes and set up mist nets. We then attracted pairs to the nets by playing the duets of wrens. To see how neurons responded during duets, we surgically implanted very small wires into a specific region of the brain, called HVC. Neurons in this region are responsible for producing the song—that is, they are premotor—and they also respond to auditory signals. To transmit the neural signals (i.e., action potentials) to a computer, a small wireless digital transmitter was then connected to the wires. We then had to wait for the birds to sing their remarkable duets.
During duet singing, there was an increase in the number of action potentials when each bird sang its part of the duet. A similar finding was made recently in another duetting bird from Africa, the white-browed sparrow-weavers. However, we found when each bird heard its partner, the number of action potentials decreased below baseline; that is, the brain was inhibited.
In a final set of experiments, as an indirect test that HVC was inhibited while hearing the partner, the birds were anesthetized with a substance that blocks inhibitory neurotransmission in the brain. With inhibition blocked, hearing the partner’s syllables produced an increase in the number of action potentials in HVC. This experiment gave us additional evidence that auditory cues from the partner, revealed under anesthesia, inhibit the song premotor circuitry in HVC when the birds are awake.
Inhibition is an interesting mechanism for turn-taking as it prevents the two birds from singing over each other. In addition, similar to bouncing on a trampoline, the inhibition creates the ability to “rebound,” or respond more quickly, which may contribute to the rapid alternation of syllables. Taken together, the alternating activity between the two birds is driven by an auditory link between the two individuals. That is, there is an increase in activity in the female HVC which produces her syllable. This signal is perceived by the male and inhibits activity in HVC, preventing him from singing. HVC activity then rebounds, and HVC is very active, producing the male syllable, which in turn is perceived by the female and inhibits her brain. Similarly, during a Zoom call with auditory delays, our brains are inhibited when we finally hear what someone is saying. This disrupts our speech pattern and makes taking turns more difficult.
This study also suggests that when individuals are interacting in a shared behavior they act as a single entity. This concept is important for any group of organisms cooperating to produce a shared behavior that is more than the sum of its parts; for example, people dancing the tango, or several people playing in band. To coordinate their behavior, the brains of all participants must link together to become a single unit.
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