Age at deafening affects the stability of learned song in adult male zebra finches

Abstract

Male zebra finches (Taeniopygia guttata) master the imitation of a song model 80-90 d after hatching and retain it with little change for the rest of their lives. Acquisition and maintenance of this imitation require intact hearing. A previous report showed that male zebra finches deafened as adults start to lose some of the acoustic and temporal features of their song a few weeks after deafening and that by 16 weeks the learned song is severely degraded (Nordeen and Nordeen, 1992). However, this previous study noted no correlation between the age at deafening and the subsequent timing and extent of song loss. We deafened adult male zebra finches ranging in age from 81 d to 6 years. The song of birds deafened at the younger ages (81-175 d) deteriorated severely after a few weeks, and within that age bracket, the older the bird was at deafening, the longer it took for this degradation to occur and the slower the subsequent process of song deterioration. The song of birds deafened at 2 years and older showed little change during the first 51 weeks after deafening but was grossly altered by 100 weeks. We suggest (1) that this age effect could be independent of experience or (2) that each time a bird sings, a little bit of learning-motor engrainment-occurs, adding to memory duration in a cumulative manner.

Fig. 1.

Typical zebra finch song structure, as revealed by sound-spectrographic analysis. Top, The motif is usually preceded by an introductory note (labeled i) repeated a variable number of times. The motif itself consists of a series of discrete sounds, usually delivered in the same order, that we call syllables and that are numbered here 1–9. Syllables have a distinct acoustic structure, with a beginning and end marked by a silent interval, as in syllables 1 and2, or by an abrupt change in frequency modulation, as insyllables 7–9. Clusters of syllables (e.g.,syllables3–6 and 7–9) separated from previous and subsequent sounds by a longer silent interval (>10 msec) are called chunks. The motif is usually repeated a number of times, forming a bout (see Fig. 9). Bottom, Repetitions of the motif, shown here at the beginning of three successive song bouts, are presented. Notice that with the exception of the variability in the number of introductory notes, the fine structure of the motif is highly stereotyped.

Fig. 2.

A–C, Song stability in three intact adult zebra finches over a long period of time. The long calls for two of these birds (B, C) are also shown. The two renditions of the song or call of the same bird have been aligned vertically to facilitate comparison of temporal and acoustic features. Each bird was at least 6 months old at the time of the first recording. As shown by the dates printed above each song, 4–5 years elapsed between the first and second recordings shown. Overall, the learned vocalizations changed relatively little in time. However, notice that some flexibility in song production is possible even with a closed-ended learner such as the zebra finch. One of the birds (A) produced two alternate, yet closely related, versions of the same motif, which differed in the last one or two syllables (arrows), an idiosyncrasy that persisted over the years. The kinds of changes that occurred over time were, for example, slight changes in harmonic emphasis (e.g., A,lastsyllable), the addition of the short call (B, arrow) or long call (C, arrow) at the end of the motif, and small changes in the temporal structure of the motif (C, notice the misalignment of the songs).

Fig. 3.

Quantification of song stereotypy in young (81–111 d of age) and old (931–2090 d of age) hearing adults.A, Mean of the means of SC and SL measures, based on 20 songs from each bird. Error bars correspond to SEs.B, Stereotypy of chunk durations. SDs were calculated from 15 repetitions of a chunk sung by a given bird; theverticalbars depict the mean of these eight SDs for each age group. Error bars are the SEs among birds in an age group. There was not a statistically significant difference between the groups.

Fig. 4.

Graph of song stereotypy as a function of age in intact adults. Stereotypy here was measured using the song analysis algorithm developed by Tchernichovski et al. (2000) (see Materials and Methods). Each bird was scored on the variability it showed in repeating 15–25 renditions of its song motif. Had all repetitions been identical, the similarity score would have been 98–99%. For each bird, each rendering of that bird's motif was compared against each of the other renderings using the “compare two songs” feature in the song analysis software; as a result, each data point shown in this graph represents the mean of 91–300 comparisons of a total of 21 birds recorded at the ages shown. Error bars indicate SEMs.

Fig. 5.

Sound-spectrographic representations of song degradation in three birds, deafened at 81 d (Young), 175 d (Middle-aged), and 2090 d (Old) after hatching. Degradation of the long call is shown for two of these birds (Young,Old). The time after deafening is indicated for each of the songs. A continuoushorizontalline is below the most complete rendering of each bird's song motif before deafening and after deafening for as long as that motif can be easily recognized. Notice that eventual degradation occurs in all three birds, but the onset, extent, and time course differs with the age at deafening. This observation, scored for all 16 birds in this experiment, is shown below (see Fig. 6). For purposes of comparison (this figure, see Fig. 6), the SSI for the last recording of the young, middle-aged, and old birds shown in this figure was 0.0, 0.6, and 2.8, respectively.

Fig. 6.

A, Song similarity index scores for all birds in this experiment plotted against time after deafening.Colors are used to identify adults that were young (red), middle-aged (blue), or old (black) at the time of deafening. Notice that song degradation, indicated by a declining similarity index, was greater and occurred faster in the birds deafened at the younger adult ages; birds deafened when they were older showed a slower decline.B, Mean similarity index scores for intact controls (whitebar) and for the different postsurgery intervals for birds deafened as young or middle-aged adults (redbars) or as old adults (blackbars). Birds in the two experimental groups were recorded at specified intervals after deafening, as shown in the box to theright of the figure. In each group'shistogram, these intervals become longer fromleft to right, corresponding to thetop to bottom listing inside thebox. The mean control score is very conservative in that it compared songs from the same individual recorded 2–5 years apart. Error bars indicate the SEM. An asteriskindicates significance at the level of p < 0.02 or better with respect to controls. Deaf., Deafening.

Fig. 7.

Postdeafening changes in chunk duration (in milliseconds) in one young adult and one old adult. Thefirstdatapoint in each series is the presurgery chunk duration; thus all pointsare shifted by 1 week. In these examples, the young bird had three chunks; the older bird had four. Notice that chunk duration changed more in the younger than in the older adult and that when changes occurred, they could be in the direction of making a chunk longer or shorter. The slope of regression lines fitted to each bird's performance during the first 8 postoperative weeks was calculated and used to produce the next figure (see Fig. 8).

Fig. 8.

“Chunk slopes,” in milliseconds per week, were determined by the absolute values of changing chunk duration (see Materials and Methods). These slopes reflect changes in chunk duration during the first 8 weeks after deafening; the larger the magnitude of the slope, the more chunk duration changed. Each bird is represented by a singlesymbol, and the code is as follows: ●, young adult (n = 6); ▪, middle-aged adult (n = 3); and −, old adult (n = 7). The slope of the young birds is consistently above that of the other two age groups. The highest value corresponds to a bird deafened at 81 d of age.

Fig. 9.

Bouts of directed song from an adult bird deafened at 1170 d recorded before (top) and 94 weeks after (bottom) deafening. The repeated unit isunderlined in each case. Notice that although the degraded song (bottom) included a motif that was shorter than its preoperative version, it was nonetheless repeated in a rather consistent manner. Consistency in the production of a degraded song was typical of most postoperative recordings.

Fig. 10.

Results of a deafening operation done in two steps. A, The left cochlea was removed when the bird was 86 d old. B, The right cochlea was removed at 231 d of age, which falls between the age ranges of the middle-aged and old birds shown in Figure 5. The time after each surgery is shown for each recording. Notice that there were no song changes after the first operation but song degraded after the second operation at a rate intermediate between what would have been expected from the middle-aged and old birds shown in Figure 5. (This bird is represented on the graph in Fig. 6 where its age at deafening, 231 d, corresponds to that when the second cochlea was removed.) This bird's long call appears at the end of the song motif. Although the long call was unaffected by the first operation, it too had deteriorated by 60 weeks after removal of the second cochlea. Theasterisk at the bottom inA marks the long call of an unseen female zebra finch used to elicit long-call responses from the male. This bird's single cochlea permitted him to hear, process, and respond to this female's long call at 16 weeks after surgery.