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

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

Auditory–vocal mirroring in songbirds

“…Despite evidence indicating that feedback shapes HVC auditory selectivity, a significant challenge to this STDP model is that the singing-related action potential activity of HVC X cells is entirely insensitive to feedback perturbations [37,38]. Moreover, studies from our group using intracellular recordings in singing birds also reveal that the singingrelated synaptic activity of HVC X cells is unaltered by acute manipulations of auditory feedback [57]. Thus, how and when auditory feedback-related information impinges on HVC remains unclear.…”

“…Interestingly, while most HVC X neurons in anaesthetized songbirds display strong and selective auditory responses, less than half of HVC X cells that display singing-related activity also respond to song playback during periods of quiet wakefulness [35,38,73,74]. Furthermore, studies in adult zebra finches reveal that auditory activity can only be detected in HVC X and most other HVC cells when the animal is sedated, anaesthetized or asleep [57,62,63,77]. Indeed, auditory responses in the HVC of sedated zebra finches are strongly suppressed by arousing stimuli, such as a brief air puff delivered to the bird's chest [62].…”

“…One explanation for this behaviour is that these cells respond to auditory feedback during singing and to similar auditory cues when the BOS is played through a speaker. However, the singing-related activity of these cells is unperturbed by acoustic manipulations that disrupt auditory feedback, suggesting that HVC X cells switch from auditory to purely motor-related activity as the bird transitions from listening to singing [38,57]. Therefore, HVC X cells display a temporally precise form of auditoryvocal mirroring that could be well suited to facilitate song learning and perception.…”

“…B 369: 20130179 suitable captive breeding habits, with the consequence that there has been some uncertainty as to whether auditoryvocal mirroring is a common feature of HVC X cells across species. Recent experiments from our own laboratory have used longitudinal recordings across the sleep-wake boundary to establish that precise auditory -vocal mirroring also is a trait of HVC X cells in male zebra finches [57]. Thus, although the auditory responses of HVC X cells are more tightly regulated by behavioural state in zebra finches than in swamp sparrows and Bengalese finches, auditory -vocal mirroring appears to be a common trait of this cell type in a wide variety of songbird species.…”

Whole-Cell Recording in the Awake Brain

“…The recordings could survive severe mechanical disturbances and remain stable for 20 min while rats explored their environment freely. Other groups have shown that sharp intracellular recordings could be obtained and maintained in freely moving birds (Long et al 2010;Hamaguchi et al 2014;Kosche et al 2015;Vallentin and Long 2015) and mice (English et al 2014;Schneider et al 2014) using a head-mountable linear microdrive. The first such recordings were made from bird premotor HVC neurons to measure the subthreshold membrane potential dynamics during singing, and the resulting recordings supported a synaptic chain-like mechanism for birdsong generation (Long et al 2010).…”