Neurophysiological coordination of duet singing

Abstract

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.

Keywords: closed-loop control; cooperation; reciprocal inhibition; sensorimotor integration; turn taking.

Fig. 1.

Neural control of solo and duet singing in plain-tailed wrens. (A) Spectrogram of a singing bout that included male solo syllables (blue line, top) followed by a duet. Solo syllables for both sexes (only male solo syllables are shown here) are sung at lower amplitudes than syllables produced in duets. Note that the smeared appearance of wren syllables in spectrograms reflects the acoustic structure of plain-tailed wren singing. (B and C) Each bird has a motor system that is used to produce song and sensory systems that mediate feedback. (B) During solo singing, the bird hears its own song, which is known as autogenous feedback (orange). (C) During duet singing, each bird hears both its own singing and the singing of its partner, known as heterogenous feedback (green). The key difference between solo and duet singing is heterogenous feedback that couples the neural systems of the two birds. This coupling results in changes in syllable amplitude and timing in both birds.

Fig. 2.

HVC neurophysiology in two pairs of wrens. In pair 1, the duet was immediately preceded by a male solo syllable. In pair 2, the duet was immediately preceded by female solo syllables. Background shading indicates which bird sang each syllable: light blue for male and light magenta for the female. Dotted lines highlight repetitions of duet motifs (repeated sequences of syllables). (A) Neural activity in awake, singing wrens. Each row of raster marks indicates the time of action potentials from each of the four electrodes implanted in each bird (blue for male, magenta for female). Between the raster plots are normalized histograms of spiking activity. The histogram for activity in the male has been inverted to highlight the temporal relations in HVC activity between the two birds. (B) Spectrogram of solo syllables and duets produced by the pairs of wrens. Lowercase blue letters are for male syllables, and uppercase magenta letters are for female syllables. The motif for pair 1 was ABcDe, and that for pair 2 was ABCdEf. (C) Neural responses to playback of the song (B) after the wrens were anesthetized with urethane. Each row in the raster plots shows spike times from a playback. (For pair 1, rasters are shown for 30$/$77 song playbacks to male and 30$/$52 playbacks to female; for pair 2, rasters are shown for 30$/$53 for male and 30$/$63 for female.) Between the raster plots are normalized peristimulus time histograms (PSTHs).

Fig. 3.

HVC activity during solo and duet singing. Negative RSs (i.e., inhibition) are highlighted in gray. A–D show mean and SD of HVC RS (firing rate during syllables minus spontaneous firing rate) across syllables before and after ($\pm$250 ms) syllable onsets. (A) RS of male HVC (blue) and of female HVC (magenta) aligned to the beginning of male solo syllables. (B) Same as A but for HVC RS aligned to the beginning of female solo syllables. (C) RS of male and female HVC aligned to the onset of male duet syllables (female syllable precedes male syllable). (D) Same as C but for RS aligned to the onset of female duet syllables. (E) Median ($+$95% CI) RS of HVC during autogenous syllables in females (left two bars) and males (right two bars). Different symbols represent different pairs of wrens, and different colors represent different duets. The color of x-axis labels indicates the sex of the bird producing the syllables. (F) Same as E but median RS ($-$95% CI) in HVC during heterogenous syllables. *Significant difference from zero (P $<$ 0.05, Wilcoxon signed-rank test).

Fig. 4.

HVC activity in response to playback of solo and duet syllables in urethane-anesthetized wrens. Negative RSs are highlighted in gray. Magenta bars (left two bars) represent median RS $+$ 95$\%$ CI in females, and blue bars (right two bars) represent it in males. Orange labels indicate playback of autogenous syllables, and green labels indicate playback of heterogenous syllables. Black asterisks indicate significant difference from zero (P $<$ 0.05, Wilcoxon signed-rank test). (A) RS in female and male HVC in response to playback of male solo and duet syllables. Dark gray asterisks at the top indicate significant differences between responses to solo and duet syllables (P $<$ 0.05, Mann–Whitney U). Symbols are the same as in Fig. 3. (B) RS in female and male HVC in response to playback of female solo and duet syllables.