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Research ArticleNew Research, Cognition and Behavior

Dopamine Depletion Affects Vocal Acoustics and Disrupts Sensorimotor Adaptation in Songbirds

Varun Saravanan, Lukas A. Hoffmann, Amanda L. Jacob, Gordon J. Berman and Samuel J. Sober
eNeuro 24 May 2019, 6 (3) ENEURO.0190-19.2019; https://doi.org/10.1523/ENEURO.0190-19.2019
Varun Saravanan
1Neuroscience Graduate Program, Graduate Division of Biological and Biomedical Sciences, Laney Graduate School, Emory University, Atlanta, GA 30322
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Lukas A. Hoffmann
1Neuroscience Graduate Program, Graduate Division of Biological and Biomedical Sciences, Laney Graduate School, Emory University, Atlanta, GA 30322
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Amanda L. Jacob
2Department of Biology, Emory University, Atlanta, GA 30322
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Gordon J. Berman
2Department of Biology, Emory University, Atlanta, GA 30322
3Department of Physics, Emory University, Atlanta, GA 30322
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Samuel J. Sober
2Department of Biology, Emory University, Atlanta, GA 30322
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Figures

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  • Figure 1.
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    Figure 1.

    Songbird neuroanatomy and experimental design. A, A theory for the role of dopamine in sensorimotor learning in songbirds. The left panel shows the brain nuclei in the songbird primarily involved in song production and learning. Area X, a songbird basal ganglia nucleus critical for song learning, receives dense dopaminergic projections from the VTA/SNc complex. The right panel shows the nuclei involved in auditory processing in the songbird. There are other inputs (data not shown) to the VTA/SNc complex from auditory areas and the ventral basal ganglia (vBG). One of the known pathways for auditory information to influence song learning is through the dopaminergic projections to Area X. We target these projections when we perform 6-OHDA lesions into Area X as depicted. B, A schematic for how the custom-built headphones introduce a pitch shifted auditory error to the birds. Briefly, a cage microphone records all sounds made within the cage and sends it through a pitch shifting program which is subsequently played back to the bird through miniature speakers attached to the headphones. The headphones also have an internal microphone to record output from the headphones speakers and to calibrate sound intensity. C, A detailed timeline for each of our experiments (see Materials and Methods).

  • Figure 2.
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    Figure 2.

    Metric for quantifying the extent of our lesions in our population of birds. We used an OD ratio between Area X and the surrounding basal ganglia (see Materials and Methods) and compared the cumulative ratios between a saline-injected population (N = 4 birds) and our 6-OHDA lesioned population (N = 16 birds). A, Examples of 6-OHDA lesioned (left) and saline-injected (right) sections. The red trace demarcates the Area X boundary. The blue circle is chosen to represent a uniformly stained section of the rest of the striatum. The ratio for each section is calculated as the OD ratio between these two regions. B, Cumulative distribution plots for the saline-injected birds (black trace) and the 6-OHDA lesioned birds (red trace). The shaded portion represents ratios that are greater than the 5th percentile for the saline-injected birds. By this metric, 37.5% of all 6-OHDA lesioned sections have a smaller OD ratio. The black and red symbols correspond to the examples shown in A. The * represents a statistically significant difference between the red trace and the black trace (Kolmogorov–Smirnov test; p < 0.05; see Results for full description).

  • Figure 3.
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    Figure 3.

    Quantifying the effect of headphones without any pitch shifts on the average change in pitch of the bird with or without lesions. A, Mean change in pitch of song for two unlesioned birds with headphones but no shifts through the headphones (reproduced from Sober and Brainard, 2009, their Supplemental Fig. 6). B, Mean change in pitch for 6-OHDA lesioned birds combining both birds with headphones but no shift in pitch (N = 5 birds) or without headphones (N = 3 birds) for a total of eight birds. The group averages for the two groups and the individual traces for all eight birds is shown in Extended Data Figure 3-1. N.S. represents not significantly different from zero, while the * represents a significant difference when comparing the last 3 d of shift combined from zero (p < 0.05).

  • Figure 4.
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    Figure 4.

    Change in pitch in response to pitch shift errors through the headphones in unlesioned and 6-OHDA lesioned birds. A, Change in pitch from baseline over the period of pitch shift for unlesioned birds broken up by the direction of introduced shift in pitch (data reanalyzed from Sober and Brainard, 2009). The graph shows that birds increase their pitch over time in response to a downward pitch shift (red trace; N = 3 birds) and decrease their pitch to an upwards pitch shift (blue trace; N = 3 birds). Traces for individual birds are shown in Extended Data Figure 4-1A. B, Same graph as in A quantified for 6-OHDA lesioned birds (N = 4 birds for each trace). Individual birds are shown in Extended Data Figure 4-1B. C, Adaptive change in pitch (see Results) for unlesioned birds (black trace; N = 6 birds) and 6-OHDA lesioned birds (gray trace; N = 8 birds). For A, B, the * and N.S. in black represent significant and not significant differences, respectively, between the two shift conditions, while the color coded differences check difference of each group from zero (see Results; Table 1).

  • Figure 5.
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    Figure 5.

    Analysis of change in pitch during washout for lesioned and unlesioned birds. A, Mean change in pitch during washout for lesioned birds with headphones but no pitch shift (N = 5 birds). Day 0 refers to the last day of the shift period. Pitch shift is turned off at the end of this day. Individual bird traces are shown in Extended Data Figure 5-1A. B, Mean change in pitch during washout for unlesioned birds (N = 3 birds for each trace). Individual bird traces are shown in Extended Data Figure 5-1B. C, Mean change in pitch during washout for 6-OHDA lesioned birds (N = 2 birds for each trace). The extremely large error bars are due in part to the bimodal nature of the data (see individual birds in Extended Data Fig. 5-1C). The statistical tests check the last 3 d of the shift period against the last 2 d of washout with * representing a significant difference (p < 0.05) and N.S. representing not significant (see Results for full tests).

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    Figure 6.

    Results when measuring the dynamics of the change in pitch or Δ(Pitch) during washout by subtracting out the pitch change on the last day of shift through the washout period. A, Δ(Pitch) during washout for lesioned no shift birds (N = 5 birds). B, The same analysis as in A for unlesioned birds subjected to ±1 semitone shift (N = 3 birds each). C, The same analysis as in A for lesioned birds subjected to ±1 semitone shift (N = 2 birds each). The * and N.S. refer to a significant difference versus not, respectively, for each group compared to zero over the last 2 d of washout.

Tables

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    Table 1.

    Statistical tests summary

    Hypothesis tested, Bayesian probability of group on left being >= column heading (see Materials and Methods, Hypothesis testing with bootstrap)
    Groups comparedZeroLesioned +1 semitone shiftLesioned –1 semitone shift
    Lesioned 0 shift0.00290.910.62
    Lesioned +1 semitone shift0.00400.26
    Lesioned –1 semitone shift0.0747
    • Results of statistical tests for ±1 semitone shift and 0 shift lesioned groups. The probabilities for each hypothesis are reported by testing the probability of the group on the left being greater than or equal to the various column headings. Blank spaces represent tests that either do not make sense to make or have been reported on another row. The probabilities that are statistically significant at α = 0.05 are depicted in bold.

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    Table 2.

    Correlations between lesion extent and changes in song metrics

    Lesion extent versusPearson’s correlation, rCorrelation significance, p
    Final pitch change0.42610.1466
    Baseline variance0.2960.3261
    Final variance–0.04980.8716
    Percent increase in variance–0.42720.1454
    • The lesion extent for each bird was defined as the proportion of sections with OD ratio below the 5th percentile of OD ratios for the population of saline-injected birds. A Pearson’s correlation coefficient (r) and the associated p value is reported for this lesion extent versus changes in song metrics. Variances were computed across either 3 d of baseline or the final 3 d of the shift period.

Extended Data

  • Figures
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  • Extended Data Figure 3-1

    A, Mean change in pitch for 6-OHDA lesioned birds either with headphones but no shift in pitch (black trace; N = 5 birds) or without headphones (gray trace; N = 3 birds). B, Mean change in pitch for individual lesioned birds subjected to zero pitch shift either with or without headphones. Download Figure 3-1, EPS file.

  • Extended Data Figure Extended Data 4-1

    A, Mean change in pitch for individual unlesioned birds subjected to a ±1 semitone pitch shift. B, Mean change in pitch for individual lesioned birds subjected to a ±1 semitone pitch shift. Note that one bird subjected to a +1 semitone shift has a discontinuity at shift day 12 since the bird did not sing at all that day. Download Figure 4-1, EPS file.

  • Extended Data Figure 5-1

    Washout traces for individual birds. A, Individual birds that had a 6-OHDA lesion, with headphones but no pitch shift. Each color is a separate bird. B, Washout traces for individual birds that were unlesioned and subjected to a ±1 semitone pitch shift. C, Washout traces for individual 6-OHDA lesioned birds subjected to a ±1 semitone pitch shift. Download Figure 5-1, EPS file.

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Dopamine Depletion Affects Vocal Acoustics and Disrupts Sensorimotor Adaptation in Songbirds
Varun Saravanan, Lukas A. Hoffmann, Amanda L. Jacob, Gordon J. Berman, Samuel J. Sober
eNeuro 24 May 2019, 6 (3) ENEURO.0190-19.2019; DOI: 10.1523/ENEURO.0190-19.2019

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Dopamine Depletion Affects Vocal Acoustics and Disrupts Sensorimotor Adaptation in Songbirds
Varun Saravanan, Lukas A. Hoffmann, Amanda L. Jacob, Gordon J. Berman, Samuel J. Sober
eNeuro 24 May 2019, 6 (3) ENEURO.0190-19.2019; DOI: 10.1523/ENEURO.0190-19.2019
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Keywords

  • basal ganglia
  • Bengalese finch
  • dopamine
  • sensorimotor adaptation
  • songbird
  • vocal learning

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