Moseley Samantha M, Meliza C Daniel
Department of Psychology, University of Virginia, Charlottesville VA 22904, USA.
Program in Fundamental Neuroscience, University of Virginia, Charlottesville VA 22904, USA.
bioRxiv. 2025 May 23:2025.05.22.655494. doi: 10.1101/2025.05.22.655494.
Postnatal experience is critical to auditory development in vertebrates. The zebra finch () 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.
出生后的经历对脊椎动物的听觉发育至关重要。斑胸草雀（）为理解复杂的社会声学环境如何影响支持对发声交流信号感知的神经回路的发育提供了一个有价值的模型。我们之前表明，在繁殖群体丰富的声学环境中饲养的斑胸草雀（群体饲养，CR）在操作性辨别任务中的表现是仅与家人一起饲养的鸟类（成对饲养，PR）的两倍，并且我们确定了PR鸟类听觉皮层功能特性的缺陷，这可以解释这种行为差异。在这里，我们在三个发育时间点（孵化后18 - 20天、30 - 35天和90 - 110天），使用来自L区L3亚区和尾内侧巢皮层（NCM）的单单位细胞外记录，追踪了经验如何影响这些功能特性的出现。虽然CR鸟类从幼雏期到成年期表现出稳定的单单位反应特性，同时群体水平编码有所改善，但PR鸟类的神经功能却逐渐恶化。PR鸟类的缺陷在18天时就开始出现在群体指标上，到30天时单单位特性也出现缺陷，并一直恶化到成年期。这些缺陷包括尖峰波形、放电率、选择性、可辨别性、编码效率和噪声不变性的改变。值得注意的是，尽管PR鸟类正常接触雄性导师的歌声，但这些缺陷仍然出现，这表明学习唱歌的能力足够强大，足以弥补受损的听觉处理能力。我们的研究结果表明，复杂的声学环境对于解码同种发声的皮层水平听觉回路的维持和发育都是必要的。
