A mechanistic account of visual discomfort
Abstract
Much of the neural machinery of the early visual cortex, from the extraction of local orientations to contextual modulations through lateral interactions, is thought to have developed to provide a sparse encoding of contour in natural scenes, allowing the brain to process efficiently most of the visual scenes we are exposed to. Certain visual stimuli, however, cause visual stress, a set of adverse effects ranging from simple discomfort to migraine attacks, and epileptic seizures in the extreme, all phenomena linked with an excessive metabolic demand. The theory of efficient coding suggests a link between excessive metabolic demand and images that deviate from natural statistics. Yet, the mechanisms linking energy demand and image spatial content in discomfort remain elusive. Here, we used theories of visual coding that link image spatial structure and brain activation to characterize the response to images observers reported as uncomfortable in a biologically based neurodynamic model of the early visual cortex that included excitatory and inhibitory layers to implement contextual influences. We found three clear markers of aversive images: a larger overall activation in the model, a less sparse response, and a more unbalanced distribution of activity across spatial orientations. When the ratio of excitation over inhibition was increased in the model, a phenomenon hypothesised to underlie interindividual differences in susceptibility to visual discomfort, the three markers of discomfort progressively shifted toward values typical of the response to uncomfortable stimuli. Overall, these findings propose a unifying mechanistic explanation for why there are differences between images and between observers, suggesting how visual input and idiosyncratic hyperexcitability give rise to abnormal brain responses that result in visual stress.
Citation
Penacchio , O , Otazu , X , Wilkins , A J & Haigh , S M 2023 , ' A mechanistic account of visual discomfort ' , Frontiers in Neuroscience , vol. 17 , 1200661 . https://doi.org/10.3389/fnins.2023.1200661
Publication
Frontiers in Neuroscience
Status
Peer reviewed
ISSN
1662-4548Type
Journal article
Description
This publication is part of the R+D+I grant PID2020-118254RB-I00 financed by MCIN/AEI/10.13039/501100011033, by the Agencia de Gestió d’Ajuts Universitaris i de Recerca (AGAUR) through 2021-SGR-01470, and the CERCA Programme/Generalitat de Catalunya. OP was funded by a Maria Zambrano Fellowship for attraction of international talent for the requalification of the Spanish university system—NextGeneration EU (ALRC). SH was funded by a pilot award from a NIH COBRE (PG20GM103650) and salary support from a NIH R15 AREA grant (MH122935).Collections
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