Saccadic modulation of stimulus processing in primary visual cortex

James M Mcfarland,Bruce G Cumming,Daniel A Butts,Richard C Saunders,Adrian G Bondy

doi:10.1038/ncomms9110

Abstract

Saccadic eye movements play a central role in primate vision. Yet, relatively little is known about their effects on the neural processing of visual inputs. Here we examine this question in primary visual cortex (V1) using receptive-field-based models, combined with an experimental design that leaves the retinal stimulus unaffected by saccades. This approach allows us to analyse V1 stimulus processing during saccades with unprecedented detail, revealing robust perisaccadic modulation. In particular, saccades produce biphasic firing rate changes that are composed of divisive gain suppression followed by an additive rate increase. Microsaccades produce similar, though smaller, modulations. We furthermore demonstrate that this modulation is likely inherited from the LGN, and is driven largely by extra-retinal signals. These results establish a foundation for integrating saccades into existing models of visual cortical stimulus processing, and highlight the importance of studying visual neuron function in the context of eye movements.

Highlights

IntroductionRelatively little is known about their effects on the neural processing of visual inputs
Saccadic eye movements play a central role in primate vision
This is consistent with previous work showing extra-retinal modulation of V1 spontaneous activity[2,3,4,5], but appears in contrast with a range of previous studies that found minimal effects of saccades on visually evoked responses5,18–22. (Note that while Ruiz et al.[22] did show clear differences in the responses of V1 neurons to saccade-induced and flashed stimuli, most of the effect they observed was due to saccade-driven visual stimulation in the neurons’ surround, rather than extra-retinal effects like those shown here.) This discrepancy is likely due to the fact that previous studies attempted to measure perisaccadic modulation by comparing a neuron’s response to a stimulus that was either introduced into its receptive field (RF) by a saccade or flashed into its RF

Summary

Introduction

Relatively little is known about their effects on the neural processing of visual inputs We examine this question in primary visual cortex (V1) using receptive-field-based models, combined with an experimental design that leaves the retinal stimulus unaffected by saccades. We demonstrate that this modulation is likely inherited from the LGN, and is driven largely by extra-retinal signals These results establish a foundation for integrating saccades into existing models of visual cortical stimulus processing, and highlight the importance of studying visual neuron function in the context of eye movements. These models reveal a much richer interaction between saccades and visual stimuli than possible with previous studies

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Results

Conclusion