Effects of Locomotion in Auditory Cortex Are Not Mediated by the VIP Network.

Iryna Yavorska,Michael Wehr

doi:10.3389/fncir.2021.618881

Abstract

Movement has a prominent impact on activity in sensory cortex, but has opposing effects on visual and auditory cortex. Both cortical areas feature a vasoactive intestinal peptide-expressing (VIP) disinhibitory circuit, which in visual cortex contributes to the effect of running. In auditory cortex, however, the role of VIP circuitry in running effects remains poorly understood. Running and optogenetic VIP activation are known to differentially modulate sound-evoked activity in auditory cortex, but it is unknown how these effects vary across cortical layers, and whether laminar differences in the roles of VIP circuitry could contribute to the substantial diversity that has been observed in the effects of both movement and VIP activation. Here we asked whether VIP neurons contribute to the effects of running, across the layers of auditory cortex. We found that both running and optogenetic activation of VIP neurons produced diverse changes in the firing rates of auditory cortical neurons, but with distinct effects on spontaneous and evoked activity and with different patterns across cortical layers. On average, running increased spontaneous firing rates but decreased evoked firing rates, resulting in a reduction of the neuronal encoding of sound. This reduction in sound encoding was observed in all cortical layers, but was most pronounced in layer 2/3. In contrast, VIP activation increased both spontaneous and evoked firing rates, and had no net population-wide effect on sound encoding, but strongly suppressed sound encoding in layer 4 narrow-spiking neurons. These results suggest that VIP activation and running act independently, which we then tested by comparing the arithmetic sum of the two effects measured separately to the actual combined effect of running and VIP activation, which were closely matched. We conclude that the effects of locomotion in auditory cortex are not mediated by the VIP network.

Highlights

Movement has complex effects on activity in auditory cortex, and involves multiple pathways
We recorded from excitatory and inhibitory neurons in auditory cortex in awake head-fixed vasoactive intestinal peptide-expressing (VIP)-ChR2 mice (N = 10 mice; included in analysis of VIP activation and locomotion) and PVChR2 mice (N = 6 mice; included in analysis of locomotion effects only) that were allowed to run on a spherical ball (Figure 1; N = 16 mice in total)
It is clear that locomotion has prominent effects in sensory cortex, and that the net effects in auditory cortex are the opposite of those in visual cortex

Summary

INTRODUCTION

Movement has complex effects on activity in auditory cortex, and involves multiple pathways. Locomotion recruits cholinergic signaling from the basal forebrain, which targets both excitatory and inhibitory cortical neurons (Hangya et al, 2015; Nelson and Mooney, 2016) How these multiple pathways interact, and how they account for the diversity of movement effects across individual cells, remains poorly understood. The fact that VIP activation facilitates PNs in both auditory and visual cortex, but that locomotion has opposing effects in auditory and visual cortex, suggests that the mechanisms underlying movement effects in auditory cortex are more complex than the locomotionVIP disinhibitory circuit in visual cortex Both M2 and the basal forebrain convey movement-related signals to auditory cortex, the extent of convergence of this input across cortical layers, and the timescale of its strongest recruitment and influence on auditory processing, remain unknown. These results suggest that the modulatory effects of running in auditory cortex are not mediated by the VIP inhibitory network

RESULTS

DISCUSSION

EXPERIMENTAL PROCEDURES