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

Kosuke Hamaguchi,Katherine A Tschida,Inho Yoon,Bruce R Donald,Richard Mooney

doi:10.7554/elife.01833

Kosuke Hamaguchi, Katherine A Tschida + Show 3 more

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https://doi.org/10.7554/elife.01833

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Journal: eLife	Publication Date: Feb 18, 2014
Citations: 78	License type: CC BY 3.0

Affiliation: Duke Medical Center, Duke University

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.

Highlights

Many elaborate behaviors, ranging from playing a guitar to engaging in a conversation, depend on the brain’s ability to integrate performance-related auditory feedback with the output of motor circuits controlling behavior
Within HVC, a distinct type of projection neuron (HVCX) provides input to an anterior forebrain pathway (AFP) that is necessary for song learning and that is anatomically similar to corticobasal ganglia pathways in mammals (Farries and Perkel, 2002; Doupe et al, 2005)
We recorded from a total of 72 HVCX neurons in 11 birds as they engaged in spontaneous bouts of singing produced in social isolation and/or listened to playback of the bird’s own song (BOS)

Summary

Introduction

Many elaborate behaviors, ranging from playing a guitar to engaging in a conversation, depend on the brain’s ability to integrate performance-related auditory feedback with the output of motor circuits controlling behavior. Songbirds use auditory feedback to learn and maintain their vocalizations (Konishi, 1965; Price, 1979) and possess well-delineated neural circuits for singing (Nottebohm et al, 1982), providing an attractive organism in which to identify synaptic mechanisms for auditory– vocal integration. Despite important progress in identifying synaptic mechanisms of auditory-guided song plasticity (Mooney, 1992; Olveczky et al, 2005; Andalman and Fee, 2009; Roberts et al, 2010; Warren et al, 2011), how auditory feedback is integrated in the brain to affect the neural circuits for singing remains poorly understood. Various studies have shown that the output nucleus of the AFP

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