Postlearning consolidation of birdsong: stabilizing effects of age and anterior forebrain lesions

Abstract

Birdsong is a learned, sequenced motor skill. For the zebra finch, learned song normally remains unchanging beyond early adulthood. However, stable adult song will gradually deteriorate after deafening (Nordeen and Nordeen, 1992), indicating an ongoing influence of auditory feedback on learned song. This plasticity of adult song in response to deafening gradually declines with age (Lombardino and Nottebohm, 2000), suggesting that, after song learning, there continue to be changes in the brain that progressively stabilize the song motor program. A qualitatively similar stabilization of learned song can be precipitated artificially by lesions of a basal ganglia circuit in the songbird anterior forebrain (Brainard and Doupe, 2000), raising the question of whether and how these two forms of song stabilization are related. We investigated this issue by characterizing the deterioration of song that occurs after deafening in young adult birds and the degree to which that deterioration is reduced by age or by lesions of the anterior forebrain that were directed at the lateral portion of the magnocellular nucleus of the anterior neostriatum (LMAN). In most respects, LMAN lesions stabilized song to a significantly greater extent than did aging; whereas old-deafened birds eventually exhibited significant deterioration of song, lesioned-deafened birds generally did not differ from controls. The one exception was for song tempo, which was significantly stabilized by age, but not by LMAN lesions. The results indicate that LMAN lesions do not simply mimic a normal aging process, and likewise suggest that the anterior forebrain pathway continues to play a role even in the residual song plasticity that is observed after the age-dependent stabilization of song.

Fig. 1.

Schematic sagittal view of song system nuclei. The “motor pathway” (shaded) is required throughout life for song production and includes nucleus HVc, the robust nucleus of the archistriatum (RA), and brainstem nuclei that control vocal and respiratory musculature, including the tracheosyringeal subdivision of the hypoglossal nucleus (nXIIts). The “anterior forebrain pathway” (solid) forms a basal ganglia–forebrain loop that leaves the motor pathway at the level of HVc and passes successively through a nucleus of the basal ganglia (Area X), the thalamus [medial subdivision of the dorsolateral thalamus (DLM)], and the anterior forebrain (LMAN) before returning to the motor pathway at the level of RA. Field L provides auditory input to the song system via indirect connections to nucleus HVc.

Fig. 2.

Example illustrating the stable song of a normal adult zebra finch (zfa12). A shows a spectrographic representation of song recorded from a normal zebra finch at 103 d of age. B shows an example of the same bird's song recorded at 540 d of age. Individual syllables of the bird's repertoire are labeled above each song; boxesenclose the stereotyped sequence of syllables, or motif, that characterized the bird's song. Both the repertoire of syllables and the order in which they were sung remained essentially unchanged, although the rate of song delivery increased.

Fig. 3.

Example illustrating one of the larger changes to song observed after deafening (zfa4), in which the original song degraded to an unrecognizable state. A, Song at 105 d of age, immediately before deafening. B, Song from 3 d after deafening. C, Expanded time axis showing an example of syllables “b” and “c” recorded before (top) and 3 d after (bottom) deafening. After deafening the previously silent interval between the syllables was often “voiced” (arrow).D, Song from 26 d after deafening. None of the original repertoire of syllables remained recognizable at this date.E, Song from 475 d after deafening. Syllables had further degraded and now included features not normally observed in zebra finch songs from our colony. F, Expanded time axis showing examples of some abnormal syllables from songs recorded 475 d after deafening. These included upwardly sweeping frequency components (solid arrows) and brief silent intervals intercalated within short duration syllables (open arrows).

Fig. 4.

Example illustrating one of the smaller changes to song observed after deafening (zfa7), in which all original syllables remained recognizable but were spectrally degraded, and in which abnormal vocalizations were introduced into the song. A,Song at 103 d of age, immediately before deafening.B, Song from 7 d after deafening. The original syllables were preserved, but variable, low-amplitude vocalizations were also introduced into the song (*). C, Song from 41 d after deafening. In addition to the presence of abnormal vocalizations (*), the spectral structure of original syllables had begun to degrade. D, Song from 203 d after deafening. The spectral structure of original syllables had further degraded, and syllables “c” and “d” had become merged.

Fig. 5.

Another example illustrating one of the smaller changes to song observed after deafening (zfm1), in which some original syllables remained recognizable but exhibited changes both to spectral structure and to sequencing. A, Songs recorded at 395 d of age, before deafening. B, Songs from 4 d after deafening. C, Songs from 34 d after deafening. Syllable “g” was frequently dropped from the song (arrows) and, when sung, was spectrally degraded.D, Songs from 94 d after deafening. In addition to further degradation and dropping of syllable “g”, songs at this date also included other abnormalities of sequence (arrows) and introduction of abnormal syllables (*).E, Songs from 256 d after deafening. Songs exhibited a further degradation of spectral structure, more new transitions between recognizable syllables (arrows), and continued presence of abnormal syllables (*).

Fig. 6.

Changes to syllable similarity after deafening. Summary for all birds of the average similarity between syllables initially present in each bird's repertoire and syllables present 1 month after deafening (solid circles) or, for control birds (open points), 1 month after the initial recording. Data are plotted as a function of the age at which birds were deafened or, for control birds, as a function of the age at which song was initially recorded.

Fig. 7.

Overall summary of changes to syllable similarity of song at 1 month and final time points for each experimental group. Each point corresponds to an individual bird and indicates the average similarity (see Materials and Methods) between syllables from the repertoire present in the initial recording session and syllables present ∼1 month or >6 months after the indicated manipulations. Bars indicate group means and SEs. Significant differences between groups are indicated in Table 1. Control birds (cont) and deafened birds (deaf) were each divided into two groups, based on age at initial recording: young adults (Y) were between 100 and 130 d of age, and old adults (O) were between 165 d and 2 years of age. Data from the young–deafened birds are indicated by filled bars, and data from the old–deafened birds are indicated by striped bars. Birds in the “lesion” group (shaded bars) received bilateral electrolytic lesions of nucleus LMAN immediately before deafening. Birds in the “sham” group received lesions outside of the song system before deafening. All of the lesioned birds except for one (indicated by the square) were young adults at the time of the manipulation. Data from two other groups are shown for comparison: the random group indicates the average similarity present between the syllables of unrelated birds, and thenerve cut group indicates the average similarity between syllables sung before and a few days after denervation of the bird's vocal organ by bilateral transection of the tracheosyringeal nerve (Fig. 1). These two groups provide measures of the minimal expected degree of syllable similarity (dashed line).

Fig. 8.

Nature of changes to syllables after deafening. Each bar indicates the mean change (±SE) between the first and final recording session (>6 months later) for all birds in the indicated groups. A, Changes in syllable noisiness as characterized by depth of modulation of harmonic spectral structure (see Materials and Methods) for syllables that remained identifiable over time. Five young–deafened birds and one old–deafened bird were excluded because of a lack of retained syllables. B,C, Changes in noisiness and waveriness scores of spectral structure (see Materials and Methods). These measures were applied to a random sample of 50–100 syllables from each recording session. D, Changes in percentage of syllables that were judged to be abnormal based on their spectral structure.E, Changes in fundamental frequency.Asterisks indicate significant differences from age-matched controls and from birds that received lesions before deafening.

Fig. 9.

Summary of changes to the temporal pattern of song. Each point corresponds to an individual bird and indicates the similarity between the temporal pattern (see Materials and Methods) of songs from the initial recording session and songs recorded ∼1 month or >6 months after the indicated manipulations. Conventions are as in Figure 7.

Fig. 10.

Average change in duration between the first and the final recording session for unmatched syllables (A) and intervals (B). For each bird and recording session the average duration of all syllables from at least 10 songs was calculated as well as the average duration of all intervals <500 msec in duration. The average duration from the final recording session was expressed as a percentage of the average duration from the initial recording session for each bird. Bars indicate the mean (±SE) change in durations for all birds in each group.

Fig. 11.

Change in duration of matched sequences of syllables. Points correspond to individual birds and indicate the durations of identified sequences of syllables at the 1 month and final time points as a percentage of the durations of those same sequences at the initial recording. Bars indicate mean (±SE) values for all birds from each group. For comparison, data are shown illustrating the average decrease in duration of identified sequences for songs sung to another bird (directed) versus songs sung in isolation (undirected). These data derive from (1) eight birds in a published study (Sossinka and Bohner, 1980), and (2) four old control birds from the current study that were recorded in both social contexts.

Fig. 12.

Contributions of syllable and interval changes to overall changes in song tempo. A, Correlation for control birds between the change in total duration of entire identified sequences that were preserved over time and the change in duration of the matched syllables from those sequences. B,Correlation for control birds between the change in total duration of entire identified sequences that were preserved over time and the duration of the matched intervals from those sequences.C, Correlation for deafened birds between changes to total duration and changes to syllable duration. D,Correlation for deafened birds between changes to total duration and changes to interval duration.

Fig. 13.

Comparison of changes to durations as assessed by consideration of all song elements, regardless of their identity (unmatched), or only song elements that were recognizably retained (matched). For syllables (A), both measures yielded similar results for the young control (y-c), old control (o-c), and lesioned and deafened (l&d) groups. However, for the young–deafened (y-d) and old–deafened (o-d) groups, there was a greater decrease in duration when unmatched syllables were considered than when only matched syllables were considered. For intervals (B), both measures again yielded similar results for the control and lesioned groups, but for the deafened groups, increases in interval durations were greater when unmatched intervals were considered than when only matched intervals were considered.