Neural correlates of perceptual plasticity in the auditory midbrain and thalamus

Hearing is an active process in which listeners must detect and identify sounds, segregate and discriminate stimulus features, and extract their behavioral relevance. Adaptive changes in sound detection can emerge rapidly, during sudden shifts in acoustic or environmental context, or more slowly as a result of practice. Although we know that context- and learning-dependent changes in the spectral and temporal sensitivity of auditory cortical (ACX) neurons support many aspects of perceptual plasticity, the contribution of subcortical auditory regions to this process is less understood. Here, we recorded single- and multi-unit activity from the central nucleus of the inferior colliculus (ICC) and the ventral subdivision of the medial geniculate nucleus (MGV) of Mongolian gerbils under two different behavioral contexts: as animals performed an amplitude modulation (AM) detection task and as they were passively exposed to AM sounds. Using a signal detection framework to estimate neurometric sensitivity, we found that neural thresholds in both regions improved during task performance, and this improvement was driven by changes in firing rate rather than phase locking. We also found that ICC and MGV neurometric thresholds improved as animals learn to detect small AM depths during a multi-day perceptual training paradigm. Finally, we reveal that in the MGV, but not the ICC, context-dependent enhancements in AM sensitivity grow stronger during perceptual training, mirroring prior observations in the ACX. Together, our results suggest that the auditory midbrain and thalamus contribute to changes in sound processing and perception over rapid and slow timescales.

听觉是一个主动的过程，其中听者需对声音进行探测与识别，对刺激特征进行区分与辨别，并提取其行为相关性。声音探测的适应性变化可能迅速出现，如声学或环境情境的突然转变，亦或因练习而缓慢发生。尽管我们知道，与情境和学习相关的变化，如听觉皮层（ACX）神经元在频谱和时域敏感性方面的变化，支持了感知可塑性的许多方面，但对于皮层下听觉区域在此过程中的贡献，我们的理解尚显不足。在本研究中，我们在两种不同的行为情境下记录了蒙古仓鼠的下丘脑中央核（ICC）和内侧膝状体腹侧分区的单细胞和多细胞活动：动物执行幅度调制（AM）检测任务时，以及它们被动暴露于AM声音时。通过信号检测框架来估算神经计量敏感性，我们发现这两个区域的神经阈值在任务执行过程中得到提升，且这种提升是由放电率的改变而非相位锁定驱动的。我们还发现，随着动物在多日感知训练范式下学会检测小的AM深度，ICC和MGV的神经计量阈值也得到改善。最后，我们揭示在MGV而非ICC中，与情境相关的AM敏感性增强在感知训练过程中变得更加显著，这与在ACX中观察到的先前现象相呼应。综合我们的研究结果，表明听觉中脑和丘脑对声音处理和感知在快速和慢速时间尺度上的变化作出了贡献。