Short-term and long-term effects of vocal distortion on song maintenance in zebra finches

Abstract

Adult zebra finch song is irreversibly altered when birds are deprived of correct feedback by deafening or denervation of the syrinx. To clarify the role of feedback in song maintenance, we developed a reversible technique to distort vocal output without damaging the auditory or vocal systems. We implanted flexible beads adjacent to the syrinx to alter its biomechanics. Immediate song aberrations included low volume, frequency shifts, missing harmonics, and production of click-like syllables. After a few weeks, seven of nine birds stopped producing some syllables. In six of these birds, the gaps left by the silenced syllables gradually shortened, and the lost syllables did not return when beads were removed 16 weeks after treatment began. The nondeleted syllables of all birds regained their preimplant morphology, insofar as could be detected, within 9 d after bead removal. In four other birds, we removed the beads as soon as syllables were deleted, when the silent intervals were still full length. In these birds, all deleted syllables returned within 1 week. Our results indicate that both silenced syllables and syllable morphology can recover as long as the song's temporal structure is maintained, but once altered, changes in the song sequence can be permanent. A hierarchical organization of the song production system has recently been described (Margoliash, 1997). Reversible disruption of song production by our method appears to permanently alter the higher levels of the system that encode song sequence, but not the lower levels that encode individual syllable structure.

Fig. 1.

Bead (B) located in the syrinx. The bead contacts the sound-producing structures, the medial labium (ML) and the medial tympanic membrane (MTM), and it is held in place by the bronchidesmus (BD). The bird's vocalizations are distorted, most likely because the close proximity of the bead to the sound-producing structures prevents them from vibrating normally. The pressure of the bead on the ML and MTM also partially occludes the bronchi (BR), which can reduce the volume of the song. The arrowhead points in the rostral direction. Scale bar, 1 mm.

Fig. 2.

Examples of distortion of individual syllables caused by bead treatment. The first column shows the prebead morphology. Distortions seen here include alteration of harmonic structure and truncation. In addition, the fundamental frequency of B16's syllables (bottom panel) decreased. Thelast column shows the syllable morphology within the first 2 weeks after the bead was removed. Scale bar, 0.5 sec; vertical axis, 2 kHz.

Fig. 3.

Two examples of songs produced before, during, and after bead implantation showing changes in overall song structure and recovery of syllable morphology. Left panel, Song before implantation (a) was continuous, loud, and highly harmonic. Two weeks after bead insertion (b), some syllables (1 and 4) are muted, and others (5 and 6) have been silenced, leaving long gaps in the song. After bead removal (c), the song syllables have returned to very near their prebead structure, but the missing syllables have not returned, and the temporal structure of song has changed such that syllable 1 now follows syllable 4 with a normal intersyllable interval.Right side,a, Prebead song;b, song recorded 2 d before bead removal. The gap left by the deletion of syllable 5 has been almost completely elided. c, Song recorded 6 d after bead removal. Syllables 1, 3, and 4 have recovered the full spectral range of the prebead song, syllable 2 has ceased to appear as a click, and syllable 4 is no longer repeated. Scale bar and axes are identical to Figure2.

Fig. 4.

Syllables lost (and gained) during bead treatments. Open circles are syllables that were retained, filled circles are dropped syllables, thehatched symbols denote syllables that were dropped but recovered after treatment, and the square is an added syllable. The dropped syllables were contiguous in each song.a, Long-term bead birds. With the exception of C77, all birds permanently dropped the syllables that were silenced during bead treatment. b, Short-term birds. All birds recovered their deleted syllables immediately after treatment.

Fig. 5.

Cross-correlation scores between prebead songs and songs recorded during and after bead treatment, for long-term bead and sham birds. Open circles, Birds that dropped at least one syllable; solid circles, birds that did not drop syllables. Scores were averaged for each month of the treatment. The prebead value is the same-day autocorrelation for songs recorded just before bead insertion. Postbead songs were recorded between 5 and 10 d after bead removal, and the postbead cross-correlation values here correspond to the treatment cross-correlation data in Table 1. The scores at each time point were compared with those at the previous time point (Wilcoxon signed-ranks test). Significant differences (stars; p < 0.02) occurred between prebead and month one, and between month four and postbead. There was no significant difference between birds that did and did not drop syllables. The solid squares show the cross-correlation scores across the same treatment period for the sham birds, which were not significantly different from the cross-treatment scores of the bead birds (Mann–Whitney U test:N = 9, 5; U = 20.500; NS).

Fig. 6.

Duration of intersyllable interval for deleted syllables as a percentage of prebead interval. Interval duration was measured from the start of the amplitude envelope of the syllable just before a group of deleted syllables to the start of the envelope of the syllable just after the deleted group. The post-removal interval was measured 5–10 weeks after bead removal. The bird plotted withopen symbols regained his dropped syllable after the bead was removed.

Fig. 7.

Plot of number of dropped syllables versus mean spectrographic autocorrelation score for songs recorded before bead implantation. Birds with more variable songs (lower autocorrelation values) dropped significantly more syllables during the 16 week distortion period. The line indicates the least-squares linear regression that best fits the data points.

Fig. 8.

Examples of syllable deletion and interval elision in a long-term and a short-term bead bird. Vertical lines separate prebead, bead, and postbead spectrograms. In the long-term bird (a), the initial duration of the interval between the onsets of syllables 4 and 1 was 294 msec. Syllable 5 was highly distorted during the first month of treatment (second spectrogram, 317 msec intersyllable interval), and was dropped during the third month (third spectrogram, 272 msec interval). By the time of bead removal, the interval was somewhat shortened; (195 msec), and it continued to close until it reached normal syllable spacing 2 months after treatment (176 msec). Recordings were at 1 week before treatment, week 2 and 15 of treatment, and 1 week and 6 weeks after treatment. In the short-term bird (b), the pretreatment interval between the onsets of syllables 4 and 7 was 434 msec. When syllables 5 and 6 were dropped during the second week of treatment, the gap did not shorten (second spectrogram, 445 msec interval), and the syllables returned 1 week after the bead was removed (424 msec interval). Recordings were at 1 week before treatment, week 2 of treatment, and 1 week after treatment. Treatment durations are as specified in Materials and Methods. Scale bar and axes are identical to Figure 2.