Neural mechanisms for turn-taking in duetting plain-tailed wrens

Abstract

Recent studies conducted in the natural habitats of songbirds have provided new insights into the neural mechanisms of turn-taking. For example, female and male plain-tailed wrens (Pheugopedius euophrys) sing a duet that is so precisely timed it sounds as if a single bird is singing. In this review, we discuss our studies examining the sensory and motor cues that pairs of wrens use to coordinate the rapid alternation of syllable production. Our studies included behavioral measurements of freely-behaving wrens in their natural habitat and neurophysiological experiments conducted in awake and anesthetized individuals at field sites in Ecuador. These studies show that each partner has a pattern-generating circuit in their brain that is linked via acoustic feedback between individuals. A similar control strategy has been described in another species of duetting songbird, white-browed sparrow-weavers (Plocepasser mahali). Interestingly, the combination of neurophysiological results from urethane-anesthetized and awake wrens suggest a role for inhibition in coordinating the timing of turn-taking. Finally, we highlight some of the unique challenges of conducting these experiments at remote field sites.

Keywords: antiphonal; auditory feedback; birdsong; central pattern generator; duets; neuroethology.

Figure 1

Social behaviors require communication between two animals. (A) Most neural studies of song control in songbirds focus on species in which only the male sings. In these birds, the pattern for the song is generated by a central pattern generator (CPG) in the male's brain (gray circular arrow). The song is then heard by the female (lighter-blue arrow), the receiver. The song is also heard by the male (dark blue arrow), which is required for song maintenance. (B) Turn-taking in wrens requires the exchange of information between a female and male. In duetting birds, singing is controlled by a CPG in the brain of each individual. The song of one individual is heard by the other and modulates the ongoing behavior of the partner. Thus, the two animals form a single circuit for the control of turn–taking (dotted box).

Figure 2

Field recordings of plain-tailed wren songs. (A) Photo of a plain-tailed wren. (B) Plain-tailed wrens live in dense bamboo on the slopes of the Andes. Photo taken near the Yanayacu Biological Field Station and Center for Creative Studies near Cosanga, Ecuador. (C) Setting up microphones in the bamboo to record wren duets. The microphones were covered with 2L soda bottles to protect them from rain. (D) Spectrogram of the beginning of a plain-tailed wren duet captured in the field. The female first sang a syllable as part of her solo song, then the male joined the duet. In this example, the male was further away from the microphone, so his syllables are of lower amplitude and can therefore be more readily distinguished from the female syllables. Female syllables are denoted with light magenta lines, and male with dark blue lines at the top of the spectrogram. Motifs (repeated sequences of syllables) are distinguished by vertical dashed green lines. (E) Segment of a song recorded in the field in which the structure of the duet changed. The first two motifs (1,2) are the same, then the birds produced a shortened motif around 4 sec of this recording. After the shortened motif, the pair sung a different motif (a,b). Syllables and motifs are labeled as in (D). Spectrograms were rendered in Matlab (MathWorks) using the spectrogram function (95% overlap, either 512- or 1,024-point window, sample rates of 10 or 25 kHz).

Figure 3

Capture and electrophysiological recording preparation. (A) A photograph of a plain-tailed wren (pink arrow) that was caught by a mist net. (B) A female (top) and male (bottom) plain-tailed wren in captivity. (C) The first electrophysiological rig that we used for recordings in urethane-anesthetized wrens. The vibration isolation table was a large tile plate that rested on tennis balls atop cinder blocks. A mesh was placed over the rig to prevent flying insects from interfering with the recordings. Note the copper rod used for grounding to the right of the rig. (D) Electrode arrays for chronic recordings were constructed at the field station in an improvised experimental rig–visible are the temperature controller (bottom right), amplifier and recording system (center right), and microscope mounted to a door used as the table. Both (C,D) are at the Yanayacu Biological Field Station and Center for Creative Studies.

Figure 4

Differences in patterns of HVC activity in awake vs. anesthetized wrens. Background shading indicates the time each bird sang a syllable: darker blue for male and lighter magenta for the female. (A) Normalized PSTH shows HVC activity recorded from the male while duetting (singing; solid blue). (B) Inverted PSTH showing activity in response to playback (20 repetitions) of the same duet while the male was anesthetized with urethane. The histogram for activity during urethane anesthesia has been inverted to highlight the temporal relations in HVC activity when the bird is awake and singing and when the bird is anesthetized. Stars highlight increases in HVC activity near the end of partner (female) syllables. These increases in HVC activity may be inhibitory auditory responses in awake birds that are revealed by the action of urethane anesthesia. (C) Spectrogram of the duet produced by the pair of wrens. Dotted green lines highlight repetitions of duet motifs. (D,E) HVC neural activity in the female during singing and urethane as in (A,B). Stars same as in (B), but for recordings in the female.