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

Daniela Saderi,Jacob R Pennington,Charles R Heller,Stephen V David,Zachary P Schwartz

doi:10.7554/elife.60153

Daniela Saderi, Jacob R Pennington + Show 3 more

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https://doi.org/10.7554/elife.60153

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Abstract

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.

Highlights

Hearing is a dynamic process that requires integration of the sensory evidence provided by physical attributes of sound with information about the behavioral context in which auditory perception occurs (Bizley and Cohen, 2013; Fritz et al, 2007)
This study determined how pupil-indexed arousal contributes to task-related spiking activity in primary auditory cortex (A1) and inferior colliculus (IC)
Several previous studies have shown that transitioning from passive listening to active behavior leads to sizable changes in neural activity in A1 (Fritz et al, 2003; Niwa et al, 2012; Otazu et al, 2009) and IC (Ryan and Miller, 1977; Slee and David, 2015)

Summary

Introduction

Hearing is a dynamic process that requires integration of the sensory evidence provided by physical attributes of sound with information about the behavioral context in which auditory perception occurs (Bizley and Cohen, 2013; Fritz et al, 2007). Even in the absence of explicit behavior, fluctuations in neural activity are observed throughout the forebrain, including primary sensory regions (Ringach, 2009; Stringer et al, 2019) This activity is related to cognitive states such as arousal and may modulate sensitivity to sensory inputs (Fu et al, 2014; Wimmer et al, 2015). Pupil size tracks the degree of neural synchronization observed in local field potentials, which is commonly used to measure arousal (Schwartz et al, 2020; Vinck et al, 2015) While this single variable is unlikely to completely characterize such a complex phenomenon as arousal, pupil provides a window into a global brain state that is activated during demanding behaviors. This work highlights the value of accounting for multiple state variables in studies of sensory coding (Musall et al, 2019; Stringer et al, 2019), both in identifying the source of task-related effects and locating where in the sensory processing hierarchy they emerge

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