Bengalese finches Lonchura Striata domestica depend upon auditory feedback for the maintenance of adult song

Abstract

Male birds of age-limited song-learning species develop their full song repertoires in the first year of life. For this type of song learner, once song is stabilized in adulthood, it is highly stereotyped and stable over time. Traditionally, it has been believed that age-limited song learners do not depend on auditory feedback for the maintenance of adult song. A recent report, however, showed that adult song in zebra finches, age-limited learners, does change after long-term deafness. We report here that another species of age-limited learner, Bengalese finches, depends critically on auditory feedback for adult song maintenance. We surgically deafened adult males and recorded song for 12 weeks after surgery. Results show that song degraded significantly within 1 week of surgery and continued to degrade over the next 11 weeks. This represents a more rapid degradation of song than has been seen previously in age-limited species. Song deficits after deafening included a marked decrease in syllable sequence stereotypy, skewed syllable distribution within song bouts, degradation of syllable phonology, and dropped, combined, and new or unrecognizable syllables. Decreased sequence stereotypy and combined syllables appeared within 1 week of deafening and did not worsen over time. Skewed syllable distributions and syllable phonology changes appeared after 1 week and did worsen. Occurrences of dropped and new syllables appeared within 1 week and increased over time. Comparison with other species indicates that much variability exists among species in the extent to which auditory feedback is necessary for song maintenance.

Fig. 2.

Within 1 week of deafening, the birds sang with a marked degradation of syllable sequence stereotypy. A, Sound spectrograph of two song repetitions recorded preoperatively.B, Spectrograph of the same duration from the same bird recorded in A but recorded 1 week after deafening. Syllable identities are labeled with numbers below the time axis.

Fig. 1.

Normal adult Bengalese finch song was recorded from control birds 10 times over 4 months. Song was stereotyped and stable over time. A, One song repetition from recordings made from a control bird 4 weeks before the experimental birds were deafened. B, Repetition of a song from the same bird from recordings made 8 weeks later. C, Recording from the same bird 12 weeks after the experimental birds were deafened (16 weeks after the recording shown in A). Syllable identities are labeled with numbers below the time axis.

Fig. 8.

After deafening, the birds sang new or unrecognizable syllables. A, Sound spectrograph of one song repetition recorded preoperatively. B,C, D, Examples of new or unrecognizable syllables sung by the same bird recorded in A but 3 weeks after deafening. Identities of original syllables are labeled with numbers. New or unrecognizable syllables are labeled with lower case letters.

Fig. 5.

A, B, Sound spectrographs showing two different syllables from two different birds recorded preoperatively. C–H, Spectrographs of the same syllables from the same birds recorded in A andB but recorded (C, D) 2 weeks after deafening, (E, F) 6 weeks after deafening, and (G, H) 12 weeks after deafening. Black bars indicate the portion of the spectrograph containing the syllable.

Fig. 7.

Within 1 week of deafening, some originally distinct syllables were truncated and combined. A, Sound spectrograph of two different syllables from one experimental bird’s song recorded preoperatively. B, An example of the combination of the two originally distinct syllables shown inA recorded 1 week after deafening. C, An example of the same combination, also recorded 1 week after deafening, in which the order of syllables has been reversed. Syllable identities are labeled with numbers below the time axis.

Fig. 3.

Sequence stereotypy scores at each recording time were averaged for control and experimental birds. A, Scores for controls were similarly high and consistent over time.B, Scores for experimental birds were similarly high over time before deafening by cochlear removal (CR), decreased significantly by 1 week after deafening, and were similarly low between 1 and 12 weeks after deafening. The hatched bar gives the mean score (±SEM) of the random model and indicates the score for a chance configuration of syllables. By 6 weeks after deafening, stereotypy scores were not statistically different from random. Numbers below the xaxis indicate the number of weeks before or after the experimental birds were deafened. Error bars represent ± SEM; **p < 0.001, compared with predeafening scores.

Fig. 4.

Syllable distribution was significantly more skewed and variable in deafened birds. Mean H values are plotted for preoperative and postoperative recordings from experimental birds. H values decreased significantly between preoperative recordings and those made 6 weeks after deafening by cochlear removal (CR). Numbers below thex axis indicate the number of weeks before or after deafening of the birds. Error bars represent ± SEM; **p < 0.001, compared with predeafening scores.

Fig. 6.

Syllables were cross-correlated within a recording date and across recording dates. Syllables sung 2 weeks after deafening were significantly different from the same syllables sung preoperatively. A, Controls, Mean correlations for repetitions of the same syllable within recording dates. B, Deaf, Mean correlations for repetitions of the same syllable within recording dates.C, Controls, Cross-correlations of syllables from recordings made 4 weeks before and 4 and 12 weeks after the experimental birds were deafened (8 weeks and 16 weeks apart).D, Cross-correlations of the same syllables sung 4 weeks before and 1, 2, 3, 6, and 12 weeks after deafening. Numbers below thex axis indicate the number of weeks before or after the experimental birds were deafened. Error bars represent ± SEM; *p < 0.05; repeated measures ANOVA.