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Articles, Behavioral/Systems/Cognitive

Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

K. W. Nordeen and E. J. Nordeen
Journal of Neuroscience 26 May 2010, 30 (21) 7392-7400; DOI: https://doi.org/10.1523/JNEUROSCI.6181-09.2010
K. W. Nordeen
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E. J. Nordeen
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  • Figure 1.
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    Figure 1.

    Deafening-induced changes in song structure were highly variable across individuals. Data shown are daily average global similarity scores [GS1 = percentage (%) similarity * accuracy * sequential match] for each animal until the time of LMAN lesion (for birds depicted in black lines/symbols) or until song motif structure was no longer evident (birds depicted in gray lines/symbols). Two animals are not included because motif structure was absent by the first postdeaf recording (d7).

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    Figure 2.

    Deafening-induced decline in song similarity scores for birds that maintained a motif structure throughout the experiment (n = 9). By the day of LMAN lesions, the global similarity GS1 (left axis), as well as each of the component scores [percentage similarity, accuracy, and sequential match (Seq. Match); right axis], were significantly lower than their predeaf baseline. Data shown are group means ± SEM, *p < 0.005 (deaf-7 vs L0).

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    Figure 3.

    Song similarity scores for birds that did not maintain a motif structure (n = 6). By the day of LMAN lesions, global similarity GS2, and each of the component scores [percentage similarity (%Sim), accuracy (Acc)] were significantly lower than their predeaf baseline. Data shown are group means ± SEM, *p < 0.05 (deaf-7 vs L0).

  • Figure 4.
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    Figure 4.

    Bilateral LMAN lesions improved the global similarity score for birds that maintained song motif structure. Scores on L3 were significantly elevated above L0 scores, and this improvement was maintained through L28. Data shown are group means ± SEM, *p < 0.05.

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    Figure 5.

    Global similarity scores for birds that maintained motif structure. Scores on L7 were significantly higher than on L0 for all birds except 88b and 75b (gray lines/symbols). The number of days elapsed between deafening and LMAN lesion is shown parenthetically in the legend. Arrow on y-axis indicates maximum score generated from comparison of predeaf motifs from unrelated males. Data shown are daily average scores for each animal.

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    Figure 6.

    Sonograms of three representative birds (38b, 59b, 88b) recorded before deafening (top), just before LMAN lesion (middle), and 7 d after LMAN lesion. The bird on the left exhibited deafening-induced deterioration of syllable morphology (e.g., syllable nos. 4, 5, 6) that recovered after LMAN lesion. Particularly obvious is that LMAN lesions reversed deafening-induced changes in the periodicity of harmonically structured sounds (e.g., syllable 4). The bird in the middle frequently omitted syllable no. 4 in L0 songs (*) and LMAN lesion improved consistency in the production of this syllable. The bird on the right had severely degraded song by L0, and LMAN lesions did not improve similarity scores.

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    Figure 7.

    In deafened birds that maintained motif structure, the extent to which predeaf global similarity scores were recovered after LMAN lesion related to the degree of song deterioration by the time of LMAN lesion (r2 = 0.46; p < 0.05). Birds with moderate behavioral deficits recovered more of their predeaf song structure than did birds with more severely deteriorated songs.

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    Figure 8.

    In deafened birds that lacked motif structure by L0 (n = 6; black symbols), LMAN lesions did not improve GS2 scores. Also plotted are scores for two of the birds (db57b and db59b; gray symbols) shown in Figure 4 that were reanalyzed using the longer song sample analysis (see Materials and Methods). Songs of birds that lacked motif structure stabilized or continued to deteriorate after LMAN lesion, while significant behavioral recovery in the two birds that retained motif structure was confirmed by this analysis. Gray bar along y-axis indicates range of scores obtained from L0 samples of these same birds compared with predeaf templates from unrelated males. The number of days that elapsed between deafening and LMAN lesion is shown parenthetically in the legend. Data shown are daily average scores for each animal.

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    Figure 9.

    Adult deafening increased and bilateral LMAN lesions decreased variability across motifs (i.e., the CV of global similarity GS1) for birds that maintained song motif structure. For the recovered animals (n = 7), scores increased significantly after deafening (d-7 vs L0: W = 28, *p < 0.02), and LMAN lesions resulted in an overall reduction in this CV that approached statistical significance (F = 12.24, p = 0.057). Post hoc t tests revealed that the CV of GS1 scores was significantly lower on L3 than on L0 (*p < 0.05), and this effect was still evident on L84 (*p < 0.05). Although unrecovered animals (n = 2) could not be evaluated statistically, they showed a similar pattern. Data shown are group means ± SEM.

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    Figure 10.

    CV of syllable features for birds that exhibited significant recovery of GS1 similarity scores after LMAN lesions (7 birds, 36 syllables). Adult deafening increased and bilateral LMAN lesions decreased variability across syllable renditions, as indicated by significant changes in the CV of most features. Data shown are group means ± SEM. The first seven features are plotted on the left axis, and the last four features are plotted on the right axis. *p < 0.05 or %p = 0.056 for d0 vs L0, #p < 0.05 for L0 vs L7. Var, Variation.

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    Table 1.

    Means (±SEM) of song syllable features that were affected by deafening and effects of LMAN lesion on those features

    EntropyPitch goodnessVariation in entropyVariation in pitch goodnessVariation in FM
    Recovered
        d0−1.86 ± 0.10729 ± 490.54 ± 0.08287,794 ± 31,191610 ± 27
        L0−1.64 ± 0.08*639 ± 41*0.39 ± 0.06*242,937 ± 24,898*563 ± 19*
        L7−1.66 ± 0.08717 ± 50#0.47 ± 0.06#299,631 ± 35,494#597 ± 23#
    Unrecovered
        d0−1.53 ± 0.11628 ± 710.59 ± 0.09253,084 ± 53,354608 ± 35
        L0−1.29 ± 0.09*475 ± 52*0.27 ± 0.04*186,919 ± 53,956*522 ± 26*
        L7−1.34 ± 0.11498 ± 580.29 ± 0.05183,782 ± 48,252511 ± 28
    • ↵aData are shown separately for birds in which global similarity scores improved after LMAN lesion (recovered; 7 birds, 36 syllables) and those that did not improve (unrecovered; 4 birds, 17 syllables).

    • *p < 0.05 (d0 versus L0);

    • ↵#p < 0.05 (L0 vs L7).

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The Journal of Neuroscience: 30 (21)
Journal of Neuroscience
Vol. 30, Issue 21
26 May 2010
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Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit
K. W. Nordeen, E. J. Nordeen
Journal of Neuroscience 26 May 2010, 30 (21) 7392-7400; DOI: 10.1523/JNEUROSCI.6181-09.2010

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Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit
K. W. Nordeen, E. J. Nordeen
Journal of Neuroscience 26 May 2010, 30 (21) 7392-7400; DOI: 10.1523/JNEUROSCI.6181-09.2010
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