A complex social-acoustical environment supports development and maintenance in the zebra finch auditory pallium

Postnatal experience is critical to auditory development in vertebrates. The Australian zebra finch (<i>Taeniopygia castanotis</i>) provides a valuable model for understanding how complex social-acoustical environments influence the development of the neural circuits that support the perception of vocal communication signals. We previously showed that zebra finches raised by their parents in a breeding colony [colony-reared (CR)] perform twice as well in a song discrimination task as birds raised with only their families [pair-reared (PR)], and we identified functional differences within the auditory pallium of PR birds that could explain this behavioral effect. 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. Although CR birds showed stable single-unit response properties from fledging to adulthood alongside improvements in population-level encoding, PR birds exhibited changes in neural function that began emerging at 18 days for population metrics and by 30 days for single-unit properties, progressing into adulthood. These included altered spike waveforms, reduced firing rates, lower selectivity, lower discriminability, lower coding efficiency, and lower noise invariance. Notably, these functional changes occurred despite PR birds receiving normal exposure to the song of a male tutor, suggesting that plasticity supporting song memorization is dissociable from plasticity that supports recognition of conspecifics' songs. Our findings demonstrate that a complex social-acoustical environment is necessary for the development and maintenance of the cortical-level auditory circuits that decode conspecific vocalizations.<b>NEW & NOTEWORTHY</b> Young zebra finches need to hear songs and calls from many birds to maintain and develop normal auditory brain circuits. When birds are raised in impoverished social-acoustical environments, the functional properties of auditory neurons change from fledging through adulthood, losing the ability to discriminate and encode vocal signals effectively. Remarkably, these deficits occur despite normal exposure to tutor song, suggesting that song memorization and auditory perception rely on different developmental mechanisms with distinct experience requirements.