Distributed and Selective Auditory Representation of Song Repertoires in the Avian Song System

Abstract

For many songbirds, the vocal repertoire constitutes acoustically distinct songs that are flexibly used in various behavioral contexts. To investigate how these different vocalizations are represented in the song neural system, we presented multiple song stimuli while performing extracellular recording in nucleus HVC in adult male song sparrows Melospiza melodia, a species known for its complex vocal repertoire and territorial use of song. We observed robust auditory responses to natural song stimuli in both awake and anesthetized animals. Auditory responses were selective for multiple songs of the bird's own repertoire (BOR) over acoustically modified versions of these stimuli. Selectivity was evident in both awake and anesthetized HVC, in contrast to auditory selectivity in zebra finch HVC, which is apparent only under anesthesia. Presentation of multiple song stimuli at different recording locations demonstrated that stimulus acoustic features and local neuronal tuning both contribute to auditory responsiveness. HVC auditory responsiveness was broadly distributed and nontopographic. Variance in auditory responsiveness was greater among than within HVC recording locations in both anesthetized and awake birds, in contrast to the global nature of auditory representation within zebra finch HVC. To assess the spatial consistency of auditory representation within HVC, we measured the repeatability with which ensembles of BOR songs were represented across the nucleus. Auditory response ranks to different songs were more consistent across recording locations in awake than in anesthetized animals. This spatial reliability of auditory responsiveness suggests that sound stimulus acoustic features contribute relatively more to auditory responsiveness in awake than in anesthetized animals.

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing, production and learning

“…The degree to which auditory tuning in the awake bird is selective to the BOS might, however, vary with developmental age and even with the species being studied. For example, HVC neurons in juvenile zebra finches show auditory related responses to both tutor song and the bird’s own song during waking states early in development (Nick and Konishi, 2005) and recordings from HVC in Bengalese finches, starlings and several species of sparrows reveal auditory responses that are selective to the BOS in the awake animal (Margoliash and Konishi, 1985; George et al, 2005; Nealen and Schmidt, 2006; Prather et al, 2008; Sakata and Brainard, 2008; Prather et al, 2009). …”

Activity in a Premotor Cortical Nucleus of Zebra Finches Is Locally Organized and Exhibits Auditory Selectivity in Neurons but Not in Glia

“…BOS responses are equally strong over the entire HVC of zebra finches [21]; and, responses to different songs in song sparrows (birds producing multiple songs) do not vary in strength across different HVC locations [26]. However, the spatial resolution provided by metal electrodes may not be sufficient to provide evidence for or against HVC local response clustering and auditory response topographies.…”

Temporal and rate code analysis of responses to low-frequency components in the bird’s own song by song system neurons

“…Numerous electrophysiological experiments in multiple songbird species have established that the BOS is an effective stimulus throughout the forebrain song system (McCasland and Konishi 1981; Margoliash 1983; Williams and Nottebohm 1985; Doupe and Konishi 1991; Margoliash and Fortune 1992; Janata and Margoliash 1999; Nealen and Schmidt 2006; Prather et al 2008). Song system neurons actively adapt their BOS-selective auditory responses as birds develop their songs during sensorimotor learning (Volman 1993; Doupe 1997; Nick and Konishi 2005).…”