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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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Two models of auditory feedback-dependent vocal and HVC dendritic plasticity.(A) A model where deafening triggers slow changes to HVCX spines, subsequently altering AFP activity, which in turn drives vocal plasticity. In this model, LMAN lesions prevent deafening-induced song degradation but will not prevent deafening-induced changes to HVCX spines. (B) A model where deafening acts through LMAN to trigger song plasticity and also to drive changes to HVCX spines. In this model, LMAN lesions will prevent both deafening-induced song degradation and deafening-induced changes to HVCX spines.DOI:http://dx.doi.org/10.7554/eLife.01833.014
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fig7: Two models of auditory feedback-dependent vocal and HVC dendritic plasticity.(A) A model where deafening triggers slow changes to HVCX spines, subsequently altering AFP activity, which in turn drives vocal plasticity. In this model, LMAN lesions prevent deafening-induced song degradation but will not prevent deafening-induced changes to HVCX spines. (B) A model where deafening acts through LMAN to trigger song plasticity and also to drive changes to HVCX spines. In this model, LMAN lesions will prevent both deafening-induced song degradation and deafening-induced changes to HVCX spines.DOI:http://dx.doi.org/10.7554/eLife.01833.014

Mentions: Our finding that HVCX cells lack feedback-sensitive synaptic activity during singing raises the question of how deafening drives structural and functional changes to synapses on HVCX cells that precede song degradation (Tschida and Mooney, 2012). One possibility is that feedback perturbations are detected by auditory neurons indirectly presynaptic to HVCX cells, and information from these feedback-sensing cells alters synapses on HVCX cells more gradually as a prelude to the AFP-mediated error correction processes that result in vocal plasticity (Figure 7A). In this ‘feedforward model’, disrupting auditory feedback should be sufficient to induce synaptic changes in HVCX cells regardless of any downstream processes in the AFP. Another possibility is that deafening-induced changes to synapses on HVCX cells depend on downstream processes in the AFP that are known to be critical for feedback-dependent changes to song (Figure 7B). Indeed, contrary to the long-held assumption that activity only propagates from HVC to the AFP, a recent study established that activity could propagate from LMAN through recurrent circuitry to HVC (Hamaguchi and Mooney, 2012). Therefore, a remaining possibility is that deafening-induced changes to synapses on HVCX cells depend on LMAN activity and not simply on the removal of auditory feedback to HVC, as predicted by the feedforward model.10.7554/eLife.01833.014Figure 7.Two models of auditory feedback-dependent vocal and HVC dendritic plasticity.


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)

Two models of auditory feedback-dependent vocal and HVC dendritic plasticity.(A) A model where deafening triggers slow changes to HVCX spines, subsequently altering AFP activity, which in turn drives vocal plasticity. In this model, LMAN lesions prevent deafening-induced song degradation but will not prevent deafening-induced changes to HVCX spines. (B) A model where deafening acts through LMAN to trigger song plasticity and also to drive changes to HVCX spines. In this model, LMAN lesions will prevent both deafening-induced song degradation and deafening-induced changes to HVCX spines.DOI:http://dx.doi.org/10.7554/eLife.01833.014
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3927426&req=5

fig7: Two models of auditory feedback-dependent vocal and HVC dendritic plasticity.(A) A model where deafening triggers slow changes to HVCX spines, subsequently altering AFP activity, which in turn drives vocal plasticity. In this model, LMAN lesions prevent deafening-induced song degradation but will not prevent deafening-induced changes to HVCX spines. (B) A model where deafening acts through LMAN to trigger song plasticity and also to drive changes to HVCX spines. In this model, LMAN lesions will prevent both deafening-induced song degradation and deafening-induced changes to HVCX spines.DOI:http://dx.doi.org/10.7554/eLife.01833.014
Mentions: Our finding that HVCX cells lack feedback-sensitive synaptic activity during singing raises the question of how deafening drives structural and functional changes to synapses on HVCX cells that precede song degradation (Tschida and Mooney, 2012). One possibility is that feedback perturbations are detected by auditory neurons indirectly presynaptic to HVCX cells, and information from these feedback-sensing cells alters synapses on HVCX cells more gradually as a prelude to the AFP-mediated error correction processes that result in vocal plasticity (Figure 7A). In this ‘feedforward model’, disrupting auditory feedback should be sufficient to induce synaptic changes in HVCX cells regardless of any downstream processes in the AFP. Another possibility is that deafening-induced changes to synapses on HVCX cells depend on downstream processes in the AFP that are known to be critical for feedback-dependent changes to song (Figure 7B). Indeed, contrary to the long-held assumption that activity only propagates from HVC to the AFP, a recent study established that activity could propagate from LMAN through recurrent circuitry to HVC (Hamaguchi and Mooney, 2012). Therefore, a remaining possibility is that deafening-induced changes to synapses on HVCX cells depend on LMAN activity and not simply on the removal of auditory feedback to HVC, as predicted by the feedforward model.10.7554/eLife.01833.014Figure 7.Two models of auditory feedback-dependent vocal and HVC dendritic plasticity.

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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