Predictive masking of an artificial scotoma is associated with a system-wide reconfiguration of neural populations in the human visual cortex

Joana Carvalho,Remco J Renken,Frans W Cornelissen

doi:10.1016/j.neuroimage.2021.118690

Joana Carvalho, Remco J Renken + Show 1 more

Open Access

https://doi.org/10.1016/j.neuroimage.2021.118690

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Abstract

The visual brain has the remarkable capacity to complete our percept of the world even when the information extracted from the visual scene is incomplete. This ability to predict missing information based on information from spatially adjacent regions is an intriguing attribute of healthy vision. Yet, it gains particular significance when it masks the perceptual consequences of a retinal lesion, leaving patients unaware of their partial loss of vision and ultimately delaying diagnosis and treatment. At present, our understanding of the neural basis of this masking process is limited which hinders both quantitative modeling as well as translational application. To overcome this, we asked the participants to view visual stimuli with and without superimposed artificial scotoma (AS). We used fMRI to record the associated cortical activity and applied model-based analyzes to track changes in cortical population receptive fields and connectivity in response to the introduction of the AS. We found that throughout the visual field and cortical hierarchy, pRFs shifted their preferred position towards the AS border. Moreover, extrastriate areas biased their sampling of V1 towards sections outside the AS projection zone, thereby effectively masking the AS with signals from spared portions of the visual field. We speculate that the signals that drive these system-wide population modifications originate in extrastriate visual areas and, through feedback, also reconfigure the neural populations in the earlier visual areas.

Highlights

Predictive masking (PM) can be considered as a manifestation of the visual system trying to predict perceptual events
Data was thresholded by retaining the pRF models that explained at least 15% of the variance in the BOLD response in the three conditions (LCR, artificial scotoma (AS)+, AS−)
We argue that the gain field (GF) model centered at the border of the scotoma is most plausible because: 1) the visualization of the pRFs in- and outside of the ASPZ shows that all tend to shift towards the border, 2) at the level of V1, the GF model at the border has more explanatory power than the one centered on the AS, 3) the common GF model centered at the AS border performs better for V1,V2, LO1 and LO2 than the on centered on the AS, and 4) due to the pooling of information throughout the visual hierarchy, pRF shifts measured in areas beyond V1 are most likely affected by the V1 shifts

Summary

Introduction

Predictive masking (PM) can be considered as a manifestation of the visual system trying to predict perceptual events. PM is a highly heterogeneous phenomenon, which can be instantaneous, i.e. blind spot, or requiring a prolonged fixation before it occurs, i.e. artificial scotoma (AS) (Weil and Rees, 2011). Long term PM, which may share similar underlying mechanisms as short-term PM, lies at the basis of the masking of retinal lesions, which often leaves patients unaware of their partial loss of vision. Such masking results in delayed diagnosis and treatment of the disease underlying the lesions, i.e. glaucoma (Hoste, 2003; Smith et al, 2012; Spillmann and Kurtenbach, 1992)

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