Shared mechanisms of auditory and non-auditory vocal learning in the songbird brain

  1. James N McGregor  Is a corresponding author
  2. Abigail L Grassler
  3. Paul I Jaffe
  4. Amanda Louise Jacob
  5. Michael S Brainard
  6. Samuel J Sober
  1. Neuroscience Graduate Program, Graduate Division of Biological and Biomedical Sciences, Laney Graduate School, Emory University, United States
  2. Department of Biology, Emory University, United States
  3. Center for Integrative Neuroscience, University of California, San Francisco, United States
  4. Howard Hughes Medical Institute, University of California, San Francisco, United States
4 figures and 1 additional file

Figures

Schematic of songbird neural circuitry and hypotheses tested.

(a) Sagittal schematic view of songbird brain circuitry. Brain nuclei of the motor pathway – the neural circuit for vocal production – are black. Brain nuclei of the anterior forebrain pathway (AFP) …

Figure 2 with 7 supplements
Non-auditory feedback drives vocal learning.

(a) Timeline of vocal learning experiments in this example bird. The order of the auditory vs. non-auditory experiments was randomized across birds. (b) Top: spectrograms and song syllables (labeled …

Figure 2—source data 1

Source data for analyses in Figure 2.

https://cdn.elifesciences.org/articles/75691/elife-75691-fig2-data1-v2.zip
Figure 2—source data 2

Source data for analyses in Figure 2—figure supplement 5 and Figure 2—figure supplement 6.

https://cdn.elifesciences.org/articles/75691/elife-75691-fig2-data2-v2.zip
Figure 2—source data 3

Source data for analyses in Figure 2—figure supplement 7.

https://cdn.elifesciences.org/articles/75691/elife-75691-fig2-data3-v2.zip
Figure 2—source code 1

Source code for use with Figure 2—source data 1 for analyses in Figure 2B-D.

https://cdn.elifesciences.org/articles/75691/elife-75691-fig2-code1-v2.zip
Figure 2—source code 2

Source code for use with Figure 2—source data 1 for analyses in Figure 2E.

https://cdn.elifesciences.org/articles/75691/elife-75691-fig2-code2-v2.zip
Figure 2—source code 3

Source code for use with Figure 2—source data 2 for analyses in Figure 2—figure supplement 5 and Figure 2—figure supplement 6.

https://cdn.elifesciences.org/articles/75691/elife-75691-fig2-code3-v2.zip
Figure 2—source code 4

Source code for use with Figure 2—source data 3 for analyses in Figure 2—figure supplement 7.

https://cdn.elifesciences.org/articles/75691/elife-75691-fig2-code4-v2.zip
Figure 2—figure supplement 1
Rates of washout across different experimental conditions.

(a) Adaptive pitch change (measured relative to baseline) during washout from the group of birds that received no craniotomies for LMAN, 6-OHDA, or sham lesions (n = 13 experiments). Adaptive pitch …

Figure 2—figure supplement 2
Amount of pitch change on each day of cutaneous stimulation training for each individual experiment.

(a) All experiments performed in birds that did not undergo any craniotomies for LMAN, 6-OHDA, or sham lesions. Orange are experiments where upward pitch change resulted in less frequent triggering …

Figure 2—figure supplement 3
LMAN lesions and 6-OHDA injections in Area X impair auditory-driven vocal learning.

(a) Adaptive change in target syllable pitch (in semitones) during 3 days of white noise training in eight birds that did not undergo any lesions or sham operations. The probability of resampled …

Figure 2—figure supplement 4
Analysis of acute effects of cutaneous stimulation on target syllable pitch.

(a) Left: for each experiment throughout all datasets described in this article, we calculated the pitch of every catch trial that occurred during each day of cutaneous stimulation training, …

Figure 2—figure supplement 5
Results from 12 example non-auditory vocal learning experiments.

(a–l) Data from 12 example experiments from each bird that did not undergo brain operations. Each dot represents the pitch of one rendition of the target syllable. Renditions in the ‘hit’ range …

Figure 2—figure supplement 6
CDF plots showing the probability a value of pitch from a distribution falls at or below the value on the x-axis for 12 example experiments from each of the birds that did not undergo brain operations.

These are the same example experiments from Figure 2—figure supplement 5, in the same order. (a–l) show data from these example experiments. The pitch distribution on the final day of cutaneous …

Figure 2—figure supplement 7
Comparison of non-auditory vocal learning when measured in the morning and in the evening.

(a) Adaptive pitch change (in semitones) of the target syllables during cutaneous stimulation training, grouped across 13 experiments in birds that did not undergo craniotomies for LMAN, 6-OHDA, or …

Figure 3 with 2 supplements
LMAN is required for non-auditory vocal learning.

(a) Timeline for electrolytic lesions of LMAN and sham operations. (b) CV of syllable pitch pre- vs. postlesion and pre- vs. postsham. LMAN lesions induced a significant reduction in pitch CV, sham …

Figure 3—figure supplement 1
Direct comparison of CV changes and learning changes between sham and lesioned (LMAN lesioned and 6-OHDA lesioned) groups.

(a) Change in syllable CV in LMAN-lesioned and sham-operated birds. Each data point represents the CV postlesion – CV prelesion of one individual song syllable. LMAN lesions induced a significant …

Figure 3—figure supplement 2
LMAN lesion histological analysis.

(a) Example images of Nissl-stained brain tissue. Tissue from sham-operated bird on the left and tissue from LMAN-lesioned bird on the right. Red boxes highlight the locations of LMAN. (b) CDF plot …

Figure 4 with 2 supplements
Dopaminergic input to Area X is required for non-auditory vocal learning.

(a) Timeline for 6-OHDA and saline (sham) injections into Area X. (b) CV of syllable pitch pre- vs. postlesion and pre- vs. postsham. Neither dopamine lesions nor shams induced significant changes …

Figure 4—figure supplement 1
6-OHDA lesion histological analysis.

(a) Example images of TH-stained brain tissue. Tissue from sham-operated bird on the left and tissue from 6-OHDA-lesioned bird on the right. Black boxes highlight the locations of Area X. (b) …

Figure 4—figure supplement 2
Comparison of lesion magnitude and learning deficit.

(a) For each bird, the difference between the magnitude of learning, calculated at the end of 3 days of cutaneous stimulation training, prelesion vs. postlesion, compared to the magnitude of the …

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