Dissociation of task engagement and arousal effects in auditory cortex and midbrain

The brain9s representation of sound is influenced by multiple aspects of internal behavioral state. Following engagement in an auditory discrimination task, both generalized arousal and task-specific control signals can influence auditory processing. To isolate effects of these state variables on auditory processing, we recorded single-unit activity from primary auditory cortex (A1) and the inferior colliculus (IC) of ferrets as they engaged in a go/no-go tone detection task while simultaneously monitoring arousal via pupillometry. We used a generalized linear model to isolate the contributions of task engagement and arousal on spontaneous and evoked neural activity. Fluctuations in pupil-indexed arousal were correlated with task engagement, but these two variables could be dissociated in most experiments. In both A1 and IC, individual units could be modulated by task and/or arousal, but the two state variables affected independent neural populations. Arousal effects were more prominent in IC, while arousal and engagement effects occurred with about equal frequency in A1. These results indicate that some changes in neural activity attributed to task engagement in previous studies should in fact be attributed to global fluctuations in arousal. Arousal effects also explain some persistent changes in neural activity observed in passive conditions post-behavior. Together, these results indicate a hierarchy in the auditory system, where generalized arousal enhances activity in the midbrain and cortex, while task-specific changes in neural coding become more prominent in cortex.