Neural correlates of perceptual plasticity in the auditory midbrain and thalamus.

Abstract

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 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 male and female 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 largely 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.Significance statement What a listener hears depends on several factors, such as whether the listener is attentive or distracted, and whether the sound is meaningful or irrelevant. Practice can also shape hearing by improving the detection of particular sound features, as occurs during language or musical learning. Understanding how changes in sound perception arise in the brain is important for developing strategies to optimize healthy hearing, and for treating disorders in which these processes go awry. We report that neurons in the auditory midbrain and thalamus exhibit rapid shifts in sound sensitivity that depend on the sound's behavioral relevance, and slower improvements that emerge over several days of training. Our results suggest that subcortical areas make an important contribution to flexible hearing.