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Auditory synapses to song premotor neurons are gated off during vocalization in zebra finches.

Hamaguchi K, Tschida KA, Yoon I, Donald BR, Mooney R - Elife (2014)

Bottom Line: A potential site for this interaction is the song premotor nucleus HVC, which receives auditory input and contains neurons (HVCX cells) that innervate an anterior forebrain pathway (AFP) important to feedback-dependent vocal plasticity.Using intracellular recordings in singing zebra finches, we found that DAF failed to perturb singing-related synaptic activity of HVCX cells, although many of these cells responded to auditory stimuli in non-singing states.These findings support a model in which the AFP accesses feedback independent of HVC.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University Medical Center, Durham, United States.

ABSTRACT
Songbirds use auditory feedback to learn and maintain their songs, but how feedback interacts with vocal motor circuitry remains unclear. A potential site for this interaction is the song premotor nucleus HVC, which receives auditory input and contains neurons (HVCX cells) that innervate an anterior forebrain pathway (AFP) important to feedback-dependent vocal plasticity. Although the singing-related output of HVCX cells is unaltered by distorted auditory feedback (DAF), deafening gradually weakens synapses on HVCX cells, raising the possibility that they integrate feedback only at subthreshold levels during singing. Using intracellular recordings in singing zebra finches, we found that DAF failed to perturb singing-related synaptic activity of HVCX cells, although many of these cells responded to auditory stimuli in non-singing states. Moreover, in vivo multiphoton imaging revealed that deafening-induced changes to HVCX synapses require intact AFP output. These findings support a model in which the AFP accesses feedback independent of HVC. DOI: http://dx.doi.org/10.7554/eLife.01833.001.

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Summary of auditory responses of HVCx cells in non-singing states.(A) Plots of subthreshold (Vm, top row) and suprathreshold (bottom row) responses to BOS playback measured by the mean and standard deviations (SDs). N = 30 HVCX cells in total. Significance level of auditory responses are tested using either the Mann–Whitney U-test (p<0.05 using ranksum function in MATLAB) or the Ansari–Bradley test (non-parametric test of variance, p<0.05, applied only when there is no significant difference in mean. Using ansaribradley function in MATLAB.) Circles, significant cells; Crosses, non-significant cells. (B) Summary of auditory responsive cells in day and night time. Subthreshold responses: 56% in day (15/27), 91% in night (10/11). Suprathreshold responses: 42% (5/12) in day, 88% (7/8) in night. (C and D) Bar plots showing the increased strength of subthreshold (C) and suprathreshold (D) responses to BOS playback during day and night-time recordings.DOI:http://dx.doi.org/10.7554/eLife.01833.009
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fig3s1: Summary of auditory responses of HVCx cells in non-singing states.(A) Plots of subthreshold (Vm, top row) and suprathreshold (bottom row) responses to BOS playback measured by the mean and standard deviations (SDs). N = 30 HVCX cells in total. Significance level of auditory responses are tested using either the Mann–Whitney U-test (p<0.05 using ranksum function in MATLAB) or the Ansari–Bradley test (non-parametric test of variance, p<0.05, applied only when there is no significant difference in mean. Using ansaribradley function in MATLAB.) Circles, significant cells; Crosses, non-significant cells. (B) Summary of auditory responsive cells in day and night time. Subthreshold responses: 56% in day (15/27), 91% in night (10/11). Suprathreshold responses: 42% (5/12) in day, 88% (7/8) in night. (C and D) Bar plots showing the increased strength of subthreshold (C) and suprathreshold (D) responses to BOS playback during day and night-time recordings.DOI:http://dx.doi.org/10.7554/eLife.01833.009

Mentions: Although previous recordings made in anesthetized zebra finches indicate that most HVCX cells can respond to auditory stimulation, and the sample of HVCX cells that we tested with DAF is reasonably large (n = 34), it remains possible that we sampled entirely from a subset of cells that do not receive auditory input. However, we found that DAF-insensitive HVCX cells could respond to auditory presentation of the bird’s own song during periods when the bird was not singing, including during the daytime or minutes to hours into the night (Figure 3A–B; 7/8 DAF-insensitive cells showed significant subthreshold responses to BOS playback during the day, and 4/4 DAF-insensitive cells that we tracked across the day–night boundary showed significant sub- and suprathreshold responses during darkness). Moreover, the majority of HVCX cells we recorded from, including those in which we did not collect singing-related activity, displayed BOS-evoked auditory activity during the day or night (Figure 3—figure supplement 1, subthreshold responses: n = 15/27 cells in day; 10/11 cells in night; suprathreshold responses: 5/12 cells in day; 7/8 cells in night). Indeed, the increased proportion of auditory-responsive HVCX cells we detected during the night is consistent with prior extracellular studies that show auditory responses in the zebra finch HVC are strongly state-dependent (Cardin and Schmidt, 2003; Rauske et al., 2003; Nick and Konishi, 2005). Therefore, we presume that many of the DAF-insensitive cells that we recorded receive auditory input but that these inputs are not activated during singing.10.7554/eLife.01833.008Figure 3.DAF-insensitive HVCX cells can respond to auditory stimuli in non-singing states.


Auditory synapses to song premotor neurons are gated off during vocalization in zebra finches.

Hamaguchi K, Tschida KA, Yoon I, Donald BR, Mooney R - Elife (2014)

Summary of auditory responses of HVCx cells in non-singing states.(A) Plots of subthreshold (Vm, top row) and suprathreshold (bottom row) responses to BOS playback measured by the mean and standard deviations (SDs). N = 30 HVCX cells in total. Significance level of auditory responses are tested using either the Mann–Whitney U-test (p<0.05 using ranksum function in MATLAB) or the Ansari–Bradley test (non-parametric test of variance, p<0.05, applied only when there is no significant difference in mean. Using ansaribradley function in MATLAB.) Circles, significant cells; Crosses, non-significant cells. (B) Summary of auditory responsive cells in day and night time. Subthreshold responses: 56% in day (15/27), 91% in night (10/11). Suprathreshold responses: 42% (5/12) in day, 88% (7/8) in night. (C and D) Bar plots showing the increased strength of subthreshold (C) and suprathreshold (D) responses to BOS playback during day and night-time recordings.DOI:http://dx.doi.org/10.7554/eLife.01833.009
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Related In: Results  -  Collection

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fig3s1: Summary of auditory responses of HVCx cells in non-singing states.(A) Plots of subthreshold (Vm, top row) and suprathreshold (bottom row) responses to BOS playback measured by the mean and standard deviations (SDs). N = 30 HVCX cells in total. Significance level of auditory responses are tested using either the Mann–Whitney U-test (p<0.05 using ranksum function in MATLAB) or the Ansari–Bradley test (non-parametric test of variance, p<0.05, applied only when there is no significant difference in mean. Using ansaribradley function in MATLAB.) Circles, significant cells; Crosses, non-significant cells. (B) Summary of auditory responsive cells in day and night time. Subthreshold responses: 56% in day (15/27), 91% in night (10/11). Suprathreshold responses: 42% (5/12) in day, 88% (7/8) in night. (C and D) Bar plots showing the increased strength of subthreshold (C) and suprathreshold (D) responses to BOS playback during day and night-time recordings.DOI:http://dx.doi.org/10.7554/eLife.01833.009
Mentions: Although previous recordings made in anesthetized zebra finches indicate that most HVCX cells can respond to auditory stimulation, and the sample of HVCX cells that we tested with DAF is reasonably large (n = 34), it remains possible that we sampled entirely from a subset of cells that do not receive auditory input. However, we found that DAF-insensitive HVCX cells could respond to auditory presentation of the bird’s own song during periods when the bird was not singing, including during the daytime or minutes to hours into the night (Figure 3A–B; 7/8 DAF-insensitive cells showed significant subthreshold responses to BOS playback during the day, and 4/4 DAF-insensitive cells that we tracked across the day–night boundary showed significant sub- and suprathreshold responses during darkness). Moreover, the majority of HVCX cells we recorded from, including those in which we did not collect singing-related activity, displayed BOS-evoked auditory activity during the day or night (Figure 3—figure supplement 1, subthreshold responses: n = 15/27 cells in day; 10/11 cells in night; suprathreshold responses: 5/12 cells in day; 7/8 cells in night). Indeed, the increased proportion of auditory-responsive HVCX cells we detected during the night is consistent with prior extracellular studies that show auditory responses in the zebra finch HVC are strongly state-dependent (Cardin and Schmidt, 2003; Rauske et al., 2003; Nick and Konishi, 2005). Therefore, we presume that many of the DAF-insensitive cells that we recorded receive auditory input but that these inputs are not activated during singing.10.7554/eLife.01833.008Figure 3.DAF-insensitive HVCX cells can respond to auditory stimuli in non-singing states.

Bottom Line: A potential site for this interaction is the song premotor nucleus HVC, which receives auditory input and contains neurons (HVCX cells) that innervate an anterior forebrain pathway (AFP) important to feedback-dependent vocal plasticity.Using intracellular recordings in singing zebra finches, we found that DAF failed to perturb singing-related synaptic activity of HVCX cells, although many of these cells responded to auditory stimuli in non-singing states.These findings support a model in which the AFP accesses feedback independent of HVC.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University Medical Center, Durham, United States.

ABSTRACT
Songbirds use auditory feedback to learn and maintain their songs, but how feedback interacts with vocal motor circuitry remains unclear. A potential site for this interaction is the song premotor nucleus HVC, which receives auditory input and contains neurons (HVCX cells) that innervate an anterior forebrain pathway (AFP) important to feedback-dependent vocal plasticity. Although the singing-related output of HVCX cells is unaltered by distorted auditory feedback (DAF), deafening gradually weakens synapses on HVCX cells, raising the possibility that they integrate feedback only at subthreshold levels during singing. Using intracellular recordings in singing zebra finches, we found that DAF failed to perturb singing-related synaptic activity of HVCX cells, although many of these cells responded to auditory stimuli in non-singing states. Moreover, in vivo multiphoton imaging revealed that deafening-induced changes to HVCX synapses require intact AFP output. These findings support a model in which the AFP accesses feedback independent of HVC. DOI: http://dx.doi.org/10.7554/eLife.01833.001.

Show MeSH
Related in: MedlinePlus