Arousal Modulates Retinal Output

Sylvia Schröder,Nicholas A Steinmetz,Michael Krumin,Marius Pachitariu,Matteo Rizzi,Leon Lagnado,Kenneth D Harris,Matteo Carandini

doi:10.1016/j.neuron.2020.04.026

Sylvia Schröder, Nicholas A Steinmetz + Show 6 more

Open Access

https://doi.org/10.1016/j.neuron.2020.04.026

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Abstract

SummaryAt various stages of the visual system, visual responses are modulated by arousal. Here, we find that in mice this modulation operates as early as in the first synapse from the retina and even in retinal axons. To measure retinal activity in the awake, intact brain, we imaged the synaptic boutons of retinal axons in the superior colliculus. Their activity depended not only on vision but also on running speed and pupil size, regardless of retinal illumination. Arousal typically reduced their visual responses and selectivity for direction and orientation. Recordings from retinal axons in the optic tract revealed that arousal modulates the firing of some retinal ganglion cells. Arousal had similar effects postsynaptically in colliculus neurons, independent of activity in the other main source of visual inputs to the colliculus, the primary visual cortex. These results indicate that arousal modulates activity at every stage of the mouse visual system.

Highlights

The activity of sensory brain regions is influenced by the level of arousal (Busse, 2018; McGinley et al, 2015; Schneider, 2020; Shimaoka et al, 2018)
To measure retinal activity in the intact, awake brain, we imaged the synaptic boutons of retinal axons in the superior colliculus (SC) (Figures 1A–1F)
We targeted the expression of a calcium indicator (SyGCaMP6f) to the axonal boutons of retinal ganglion cells (Dreosti et al, 2009; Liang et al, 2018) in contralateral superficial SC

Summary

Introduction

The activity of sensory brain regions is influenced by the level of arousal (Busse, 2018; McGinley et al, 2015; Schneider, 2020; Shimaoka et al, 2018). In the mouse visual system, this influence has been observed in primary visual cortex (V1; Niell and Stryker, 2010), lateral geniculate nucleus (Aydın et al, 2018; Erisken et al, 2014), and superior colliculus (SC; Ito et al, 2017; Savier et al, 2019) Arousal affects both spontaneous and visually driven activity, increasing firing rates in some neurons and decreasing them in others (Erisken et al, 2014; Ito et al, 2017; Niell and Stryker, 2010; Stringer et al, 2019; Vinck et al, 2015). We developed an optical approach to measure the activity of retinal synapses during behavior, in the intact brain

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