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

Abstract

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.

Audiovisual task switching rapidly modulates sound encoding in mouse auditory cortex

“…This activity reduction is behaviorally meaningful, as error trials are predicted by higher firing rates in the set of units that is suppressed in the A-rule. Many previous studies examining behavioral modulation of AC activity have relied on comparisons between task-engaged and passive exposure conditions (Bagur et al, 2018;Carcea et al, 2017;Kuchibhotla et al, 2017;Otazu et al, 2009), which may differ in terms of arousal, attention, reward expectation, and motor activity (Saderi et al, 2021). By holding arousal, motor activity, and physical stimulus features constant between conditions, we were able to isolate attentional effects on AC activity.…”

“…AC integrates ascending auditory information with diverse input from frontal, cingulate, striatal, and non-auditory sensory areas to rapidly alter sensory processing in response to changing behavioral demands (Budinger and Scheich, 2009;Budinger et al, 2008;Park et al, 2015;Rodgers and DeWeese, 2014;Winkowski et al, 2013). To isolate the influence of modality-selective attentional modulation, we compared responses to identical compound auditory-visual stimuli within task, under different cued contexts requiring attention to the auditory or visual elements, thus holding constant other task-related variables such as arousal, attention, reward expectation, and motor activity (Saderi et al, 2021).…”

Dimensionality reduction for neural population decoding

“…N = 52 neurons were recorded simultaneously using a 64-channel laminar probe 27 as in. [28][29][30] Auditory stimuli consisting of narrowband (0.3 octave bandwidth) noise bursts were presented alone (-Inf dB) or with a pure tone embedded at varying SNRs (0 dB, −5 dB, −10 dB) in the hemifield contralateral to the recording site (see Experimental Methods). Each stimulus was repeated 50 times.…”

“…Recording procedures followed those described previously. 28,29 Briefly, upon opening a craniotomy, 1 -4 tungsten micro-electrodes (FHC, 1-5 MΩ) were inserted to characterize the tuning and response latency of the region of cortex. Sites were identified as A1 by characteristic short latency responses, frequency selectivity, and tonotopic gradients across multiple penetrations.…”

Selective effects of arousal on population coding of natural sounds in auditory cortex

“…First-order response modulation by arousal has been observed in multiple stages of the auditory pathway, even before auditory cortex. 51,52 Further, stochastic variability in the ascending auditory pathway may cause noise correlation in neurons that share ascending input. However, this seems unlikely as this type of noise has been reported to be very weak in cortex.…”