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 13 days 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.

Song Preference in Female and Juvenile Songbirds: Proximate and Ultimate Questions

“…Later, mainly in zebra finches, the neural responses were compared across ages to investigate how such neural selectivity develops. Consistent with the sensitivity to own-species song at a behavioral level, electrophysiological recordings ( Stripling et al, 2001 ; Schroeder and Remage-Healey, 2021 ) and immunohistochemical assay ( Stripling et al, 2001 ; Bailey and Wade, 2003 , Bailey and Wade, 2005 ) showed that some neurons in the NCM selectively respond to conspecific song over heterospecific song either at a single-cell level or at a population level. These results indicated that the selectivity is already present at the age of 20 days post hatch, which is said to be the beginning of the sensory learning in this species ( Roper and Zann, 2006 ).…”

A complex acoustical environment during development enhances auditory perception and coding efficiency in the zebra finch

“…CR birds also have the opportunity for vocal and visual interactions with individuals outside their family, and there may be more diffuse effects of social density on brain development 57 . It also remains to be seen to what extent the effects we observed are the result of an early sensitive period 58 or more recent plasticity 28 . Future work could begin to address these questions by controlling the timing and statistics of the acoustical background presented via loudspeaker to PR clutches.…”

Expansion of learning capacity elicited by interspecific hybridization

“…However, the potential significance of transcriptional characteristics in auditory areas for the learning outcomes observed in the F 1 hybrids and species-specific learning capacities should not be overlooked. Although a certain number of NCM neurons exhibit varying neural activities in response to conspecific and heterospecific songs ( 51 , 53 , 65 ), only specific subsets of these neurons may play a role in shaping the memory of a song model to be learned ( 52 ). Sampling from multiple auditory regions, including field L (a primary cortical auditory region) and the caudomedial mesopallium (another higher auditory region), could be useful to examine whether some observed differences in song learning capacity are due to variations in the auditory system of F 1 hybrids.…”