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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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Contingent DAF drives adaptive changes in spectral features of the target syllable.When spectral features of a syllable meet certain criteria, white noise is played to the bird. This type of contingent DAF protocol is known to induce adaptive changes in the spectral features of song (Andalman and Fee, 2009; Warren et al., 2011). The criteria used here to trigger DAF were (1) sound amplitude ∼1–5 dB above baseline and (2) a mean frequency above or below a certain threshold (orange regions in [C and D]). This frequency threshold was iteratively adjusted to induce vocal changes in the birds. (A and B) Examples of target syllables (syllable b) that did not receive DAF (A) and that received DAF (B; denoted as b’). (C) Distribution of target syllable frequency as a function of number of syllable renditions (black dots, 10 ms window measured from target onset; red line is running average of syllable frequency). (D) Mean ± SD of the target syllable frequency on each day. The mean frequency of the target syllable shifted significantly after several days of contingent DAF in both upward (day1–4) and downward (day 5–9) directions (t-test, day 1 vs day 4, day 4 vs day 7, day 7 vs day 9, p<10−33). Here, the mean frequency threshold was set to <5000 Hz (days 1–4, escape in upward shift), >5800 Hz (days 5–7, escape in downward shift), and >5400 Hz (days 8 and 9, escape in downward shift).DOI:http://dx.doi.org/10.7554/eLife.01833.006
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fig1s3: Contingent DAF drives adaptive changes in spectral features of the target syllable.When spectral features of a syllable meet certain criteria, white noise is played to the bird. This type of contingent DAF protocol is known to induce adaptive changes in the spectral features of song (Andalman and Fee, 2009; Warren et al., 2011). The criteria used here to trigger DAF were (1) sound amplitude ∼1–5 dB above baseline and (2) a mean frequency above or below a certain threshold (orange regions in [C and D]). This frequency threshold was iteratively adjusted to induce vocal changes in the birds. (A and B) Examples of target syllables (syllable b) that did not receive DAF (A) and that received DAF (B; denoted as b’). (C) Distribution of target syllable frequency as a function of number of syllable renditions (black dots, 10 ms window measured from target onset; red line is running average of syllable frequency). (D) Mean ± SD of the target syllable frequency on each day. The mean frequency of the target syllable shifted significantly after several days of contingent DAF in both upward (day1–4) and downward (day 5–9) directions (t-test, day 1 vs day 4, day 4 vs day 7, day 7 vs day 9, p<10−33). Here, the mean frequency threshold was set to <5000 Hz (days 1–4, escape in upward shift), >5800 Hz (days 5–7, escape in downward shift), and >5400 Hz (days 8 and 9, escape in downward shift).DOI:http://dx.doi.org/10.7554/eLife.01833.006

Mentions: Although previous studies have shown that singing-related action potentials of HVCX neurons are insensitive to DAF (Kozhevnikov and Fee, 2007; Prather et al., 2008), we tested whether singing-related synaptic inputs to HVCX cells encode auditory information by perturbing auditory feedback during singing. To distort the bird’s experience of singing-related auditory feedback, we used a computer-controlled real-time system to detect a specific syllable in the bird’s song motif and trigger sound playback during the production of the ensuing ‘target’ syllable (Figure 1C; ‘Materials and methods’ and Figure 1—figure supplement 2). Playback sounds included either a 100-ms noise burst or a recorded version of one of the bird’s own syllables; using either of these stimuli to distort singing-related auditory feedback has been shown to induce gradual changes to adult song, indicating the existence of neural circuitry that detects these acute feedback perturbations and induces vocal plasticity (Leonardo and Konishi, 1999; Tumer and Brainard, 2007; Andalman and Fee, 2009). To establish the efficacy of this DAF method, we set the sound amplitude slightly above the level that causes song truncation in some initial trials (∼65 dB at the center of the cage). To ensure that any changes in subthreshold activity we might detect were driven by feedback perturbations rather than by acute changes in motor-related activity, we excluded from analysis any trials in which DAF triggered truncation or changes in song tempo (see below for a description of subthreshold activity in those DAF trials that evoked acute motor effects; also see Sakata and Brainard, 2008). In separate behavioral experiments, we also confirmed that applying our perturbation protocol in a pitch-contingent manner over a period of days as previously described (Tumer and Brainard, 2007) was sufficient to shift the pitch of target syllables (Figure 1—figure supplement 3; the observed hit rate was 30–70%).


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)

Contingent DAF drives adaptive changes in spectral features of the target syllable.When spectral features of a syllable meet certain criteria, white noise is played to the bird. This type of contingent DAF protocol is known to induce adaptive changes in the spectral features of song (Andalman and Fee, 2009; Warren et al., 2011). The criteria used here to trigger DAF were (1) sound amplitude ∼1–5 dB above baseline and (2) a mean frequency above or below a certain threshold (orange regions in [C and D]). This frequency threshold was iteratively adjusted to induce vocal changes in the birds. (A and B) Examples of target syllables (syllable b) that did not receive DAF (A) and that received DAF (B; denoted as b’). (C) Distribution of target syllable frequency as a function of number of syllable renditions (black dots, 10 ms window measured from target onset; red line is running average of syllable frequency). (D) Mean ± SD of the target syllable frequency on each day. The mean frequency of the target syllable shifted significantly after several days of contingent DAF in both upward (day1–4) and downward (day 5–9) directions (t-test, day 1 vs day 4, day 4 vs day 7, day 7 vs day 9, p<10−33). Here, the mean frequency threshold was set to <5000 Hz (days 1–4, escape in upward shift), >5800 Hz (days 5–7, escape in downward shift), and >5400 Hz (days 8 and 9, escape in downward shift).DOI:http://dx.doi.org/10.7554/eLife.01833.006
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fig1s3: Contingent DAF drives adaptive changes in spectral features of the target syllable.When spectral features of a syllable meet certain criteria, white noise is played to the bird. This type of contingent DAF protocol is known to induce adaptive changes in the spectral features of song (Andalman and Fee, 2009; Warren et al., 2011). The criteria used here to trigger DAF were (1) sound amplitude ∼1–5 dB above baseline and (2) a mean frequency above or below a certain threshold (orange regions in [C and D]). This frequency threshold was iteratively adjusted to induce vocal changes in the birds. (A and B) Examples of target syllables (syllable b) that did not receive DAF (A) and that received DAF (B; denoted as b’). (C) Distribution of target syllable frequency as a function of number of syllable renditions (black dots, 10 ms window measured from target onset; red line is running average of syllable frequency). (D) Mean ± SD of the target syllable frequency on each day. The mean frequency of the target syllable shifted significantly after several days of contingent DAF in both upward (day1–4) and downward (day 5–9) directions (t-test, day 1 vs day 4, day 4 vs day 7, day 7 vs day 9, p<10−33). Here, the mean frequency threshold was set to <5000 Hz (days 1–4, escape in upward shift), >5800 Hz (days 5–7, escape in downward shift), and >5400 Hz (days 8 and 9, escape in downward shift).DOI:http://dx.doi.org/10.7554/eLife.01833.006
Mentions: Although previous studies have shown that singing-related action potentials of HVCX neurons are insensitive to DAF (Kozhevnikov and Fee, 2007; Prather et al., 2008), we tested whether singing-related synaptic inputs to HVCX cells encode auditory information by perturbing auditory feedback during singing. To distort the bird’s experience of singing-related auditory feedback, we used a computer-controlled real-time system to detect a specific syllable in the bird’s song motif and trigger sound playback during the production of the ensuing ‘target’ syllable (Figure 1C; ‘Materials and methods’ and Figure 1—figure supplement 2). Playback sounds included either a 100-ms noise burst or a recorded version of one of the bird’s own syllables; using either of these stimuli to distort singing-related auditory feedback has been shown to induce gradual changes to adult song, indicating the existence of neural circuitry that detects these acute feedback perturbations and induces vocal plasticity (Leonardo and Konishi, 1999; Tumer and Brainard, 2007; Andalman and Fee, 2009). To establish the efficacy of this DAF method, we set the sound amplitude slightly above the level that causes song truncation in some initial trials (∼65 dB at the center of the cage). To ensure that any changes in subthreshold activity we might detect were driven by feedback perturbations rather than by acute changes in motor-related activity, we excluded from analysis any trials in which DAF triggered truncation or changes in song tempo (see below for a description of subthreshold activity in those DAF trials that evoked acute motor effects; also see Sakata and Brainard, 2008). In separate behavioral experiments, we also confirmed that applying our perturbation protocol in a pitch-contingent manner over a period of days as previously described (Tumer and Brainard, 2007) was sufficient to shift the pitch of target syllables (Figure 1—figure supplement 3; the observed hit rate was 30–70%).

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