Correspondence© 2 0 2 0 S p r i n g e r N a t u r e L i m i t e d . A l l r i g h t s r e s e r v e d .

Both generalized arousal and engagement in a specific task influence sensory neural processing. To isolate effects of these state variables in the auditory system, we recorded single-unit activity from primary auditory cortex (A1) and inferior colliculus (IC) of ferrets during a tone detection task, while monitoring arousal via changes in pupil size. We used a generalized linear model to assess the influence of task engagement and pupil size on sound-evoked activity. In both areas, these two variables affected independent neural populations. Pupil size effects were more prominent in IC, while pupil and task engagement effects were equally likely in A1. Task engagement was correlated with larger pupil; thus, some apparent effects of task engagement should in fact be attributed to fluctuations in pupil size. These results indicate a hierarchy of auditory processing, where generalized arousal enhances activity in midbrain, and effects specific to task engagement become more prominent in cortex.

The brain’s 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.

In addition to encoding sound stimulus features, activity in primary auditory cortex (A1) is modulated by non-sensory behavioral state variables, including arousal. Here, we investigated how arousal, measured by pupil size, influences stimulus discriminability in A1. To do this, we recorded from populations of A1 neurons in awake animals while presenting a diverse set of natural sound stimuli. In contrast to previous work, the large stimulus set allowed us to investigate effects of arousal across a wide range of sensory response space. Arousal consistently increased evoked response magnitude and reduced pairwise noise correlations. On average, these changes improved the accuracy of the neural code. However, effects varied across stimuli; neural coding was most improved for areas of the sensory space where noise correlations interfered with the sensory discrimination axis. We also found that first-order modulation of evoked responses and second-order modulation of correlated variability acted on distinct neural populations and timescales, suggesting that arousal interacts with multiple circuits underlying activity in A1.

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