Adult-like neural representation of species-specific songs in the auditory forebrain of zebra finch nestlings.

Abstract

Encoding of conspecific signals during development can reinforce species barriers as well as set the stage for learning and production of species-typical vocalizations. In altricial songbirds, the development of the auditory system is not complete at hatching, so it is unknown the degree to which recently hatched young can process auditory signals like birdsong. We measured in vivo extracellular responses to song stimuli in a zebra finch (Taeniopygia guttata) secondary auditory forebrain region, the caudomedial nidopallium (NCM). We recorded from three age groups between 13days post-hatch and adult to identify possible shifts in stimulus encoding that occur before the opening of the sensitive period of song motor learning. We did not find differences in putative cell type composition, firing rate, response strength, and selectivity across ages. Across ages narrow-spiking units had higher firing rates, response strength, accuracy, and trial-by-trial reliability along with lower selectivity than broad-spiking units. In addition, we showed that stimulus-specific adaptation, a characteristic of adult NCM, was also present in nestlings and fledglings. These results indicate that most features of secondary auditory processing are already adult-like shortly after hatching. Furthermore, we showed that selectivity for species-specific stimuli is similar across all ages, with the greatest fidelity in temporal coding in response to conspecific song and domesticated Bengalese finch song, and reduced fidelity in response to owl finch song, a more ecologically relevant heterospecific, and white noise. Our study provides the first evidence that the electrophysiological properties of higher-order auditory neurons are already mature in nestling songbirds.