Song Decrystallization in Adult Zebra Finches Does Not Require the Song Nucleus NIf

Abstract

In adult male zebra finches, transecting the vocal nerve causes previously stable (i.e., crystallized) song to slowly degrade, presumably because of the resulting distortion in auditory feedback. How and where distorted feedback interacts with song motor networks to induce this process of song decrystallization remains unknown. The song premotor nucleus HVC is a potential site where auditory feedback signals could interact with song motor commands. Although the forebrain nucleus interface of the nidopallium (NIf) appears to be the primary auditory input to HVC, NIf lesions made in adult zebra finches do not trigger song decrystallization. One possibility is that NIf lesions do not interfere with song maintenance, but do compromise the adult zebra finch's ability to express renewed vocal plasticity in response to feedback perturbations. To test this idea, we bilaterally lesioned NIf and then transected the vocal nerve in adult male zebra finches. We found that bilateral NIf lesions did not prevent nerve section-induced song decrystallization. To test the extent to which the NIf lesions disrupted auditory processing in the song system, we made in vivo extracellular recordings in HVC and a downstream anterior forebrain pathway (AFP) in NIf-lesioned birds. We found strong and selective auditory responses to the playback of the birds' own song persisted in HVC and the AFP following NIf lesions. These findings suggest that auditory inputs to the song system other than NIf, such as the caudal mesopallium, could act as a source of auditory feedback signals to the song motor network.

Regulation of learned vocal behavior by an auditory motor cortical nucleus in juvenile zebra finches

“…What speaks against this possibility is that currently there exists no evidence that NIf conveys auditory feedback involved in song plasticity. Song decrystallization following vocal nerve transsection does not require NIf (Roy and Mooney 2009). NIf input to HVC could thus reflect auditory feedback not used for song plasticity but used for completing the ongoing song.…”

Neural mechanisms for learned birdsong

“…Because HVC is thought to be a bottleneck through which auditory information reaches the AFP (Bauer et al 2008;Roy and Mooney 2009), and because HVC RA neurons appear to lack auditory responses altogether in the awake bird , neurons whose action potential activity is sensitive to realtime feedback perturbations must be presynaptic to HVC X cells. Two recent studies provide evidence that neurons directly and indirectly presynaptic to HVC X cells can change their spiking patterns in response to real-time feedback perturbations (Sakata and Brainard 2008;Keller and Hahnloser 2009).…”

Auditory–vocal mirroring in songbirds

“…Nonetheless, a variety of evidence supports the idea that HVC is a site where a precise timing signal necessary for song motor patterning originates. Although one of HVC's major telencephalic afferents, NIf, contains neurons that may fire in a temporally precise manner during singing [86], completely ablating NIf disrupts singing for only a few days, after which the bird continues to sing normally [77,87]. And although lesions in a thalamic afferent to HVC, Uva, can permanently disrupt the song pattern [88], presumably by interfering with the bilateral coordination of HVC activity mediated through recurrent circuitry in which Uva is embedded, Uva neurons do not display singing-related activity that is precisely time-locked to the song [89].…”

“…Several of HVC's afferents contain auditory-responsive cells, and reversible inactivation studies implicate two of these-NIf and CM/Av-as the sources of much or all of the auditory drive to HVC [77,87,91,92]. Figure 4.…”

“…spike-timing-dependent plasticity; STDP) could result in precise auditory-vocal mirroring [99]. Support for an effect of feedback on the auditory properties of HVC X cells comes from the observation that BOS-selectivity in HVC and the AFP develops in parallel with the process of song imitation [43,100,101], and from the finding that exposing adult finches for prolonged periods to distorted auditory feedback can drive auditory retuning to the distorted BOS in both HVC and the AFP [53,87]. Perhaps most compellingly, in vivo multiphoton imaging reveals that deafening can destabilize and shrink dendritic spines on HVC X but not HVC RA cells, an effect that precedes and predicts the severity of subsequent song deterioration [102].…”