Moseley, S. M. | bioRxiv Science

bioRxiv2025

A complex acoustical environment is necessary for maintenance and development in the zebra finch auditory pallium

Postnatal experience is critical to auditory development in vertebrates. The zebra finch (Taeniopygia castanotis) provides a valuable model for understanding how complex social-acoustical environments influence development of the neural circuits that support perception of vocal communication signals. We previously showed that zebra finches raised in the rich acoustical environment of a breeding colony (colony-reared, CR) perform twice as well in an operant discrimination task as birds raised with only their families (pair-reared, PR), and we identified deficits in functional properties within the auditory pallium of PR birds that could explain this behavioral difference. Here, using single-unit extracellular recordings from the L3 subdivision of field L and caudomedial nidopallium (NCM) at three developmental timepoints (18-20, 30-35, and 90-110 days post hatch), we tracked how experience affects the emergence of these functional properties. Whereas CR birds showed stable single-unit response properties from fledging to adulthood alongside improvements in population-level encoding, PR birds exhibited progressive deterioration in neural function. Deficits in PR birds began emerging at 18 days for population metrics and by 30 days for single-unit properties, worsening into adulthood. These included altered spike waveforms, firing rates, selectivity, discriminability, coding efficiency, and noise invariance. Notably, these deficits occurred despite PR birds receiving normal exposure to the song of a male tutor, suggesting that learning to sing is robust enough to compensate for impaired auditory processing. Our findings demonstrate that a complex acoustical environment is necessary for both maintenance and development of the cortical-level auditory circuits that decode conspecific vocalizations.

neuroscience↗

bioRxiv2024

Cortical Processing of Conspecific Vocalizations in Zebra Finches Depends on the Early Acoustical Environment

Sensory experience during development has lasting effects on perception and neural processing. Exposing juvenile animals to artificial stimuli influences the tuning and functional organization of the auditory cortex, but less is known about how the rich acoustical environments experienced by vocal communicators affect the processing of complex vocalizations. Here, we show that in zebra finches (Taeniopygia guttata), a colonial-breeding songbird species, exposure to a naturalistic social-acoustical environment during development has a profound impact on auditory perceptual behavior and on cortical-level auditory responses to conspecific song. Compared to birds raised by pairs in acoustic isolation, male and female birds raised in a breeding colony were better in an operant discrimination task at recognizing conspecific songs with and without masking colony noise. Neurons in colony-reared birds had higher average firing rates, selectivity, and discriminability, especially in the narrow-spiking, putatively inhibitory neurons of a higher-order auditory area, the caudomedial nidopallium (NCM). Neurons in colony-reared birds were also less correlated in their tuning and more efficient at encoding the spectrotemporal structure of conspecific song, and better at filtering out masking noise. These results suggest that the auditory cortex adapts to noisy, complex acoustical environments by strengthening inhibitory circuitry, functionally decoupling excitatory neurons while maintaining overall excitatory-inhibitory balance. Significance StatementThe statistics of the sensory inputs animals experience during postnatal development shape cortical circuits and their functional properties, but most studies examining experience-dependent plasticity in the auditory system has employed artificial stimuli with limited relevance to acoustic communication. Here, we examined how the natural social-acoustical environment experienced by zebra finches, a social songbird that breeds in large colonies, influences the development of auditory perception and the underlying auditory cortical circuits. Compared to birds raised in a more impoverished environment, colony-reared birds were better at recognizing songs of other zebra finches and had higher firing rates in the avian homolog to auditory cortex, along with changes to functional connectivity that resulted in more efficient and robust coding of conspecific song.

neuroscience↗