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Visual looming is a primitive for human emotion

Looming objects afford threat of collision across the animal kingdom. Defensive responses to looming and neural computations for looming detection are strikingly conserved across species. In mammals, information about rapidly approaching threats is conveyed from the retina to the midbrain superior c...

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Autores principales: Thieu, Monica K., Ayzenberg, Vladislav, Lourenco, Stella F., Kragel, Philip A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10491236/
https://www.ncbi.nlm.nih.gov/pubmed/37693448
http://dx.doi.org/10.1101/2023.08.29.555380
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author Thieu, Monica K.
Ayzenberg, Vladislav
Lourenco, Stella F.
Kragel, Philip A.
author_facet Thieu, Monica K.
Ayzenberg, Vladislav
Lourenco, Stella F.
Kragel, Philip A.
author_sort Thieu, Monica K.
collection PubMed
description Looming objects afford threat of collision across the animal kingdom. Defensive responses to looming and neural computations for looming detection are strikingly conserved across species. In mammals, information about rapidly approaching threats is conveyed from the retina to the midbrain superior colliculus, where variables that indicate the position and velocity of approach are computed to enable defensive behavior (1). Neuroscientific theories posit that emotional feelings are based on representations in the midbrain (2), which are further elaborated in cortical systems (3). However, how these computations relate to phenomenal experience in humans is largely unknown. Here, we show that a shallow convolutional neural network based on the Drosophila visual system predicts human behavioral and brain responses across development. In laboratory experiments using controlled visual stimuli, we find that this model explains defensive behaviors to looming objects in infants and superior colliculus responses to optical expansion in adults. Further, examining responses to a broader array of naturalistic video clips, we observe that representations of looming from this model predict self-reported emotion largely on the basis of subjective arousal. Our results illustrate how human emotions may be supported by species-general systems for survival in unpredictable environments.
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spelling pubmed-104912362023-09-09 Visual looming is a primitive for human emotion Thieu, Monica K. Ayzenberg, Vladislav Lourenco, Stella F. Kragel, Philip A. bioRxiv Article Looming objects afford threat of collision across the animal kingdom. Defensive responses to looming and neural computations for looming detection are strikingly conserved across species. In mammals, information about rapidly approaching threats is conveyed from the retina to the midbrain superior colliculus, where variables that indicate the position and velocity of approach are computed to enable defensive behavior (1). Neuroscientific theories posit that emotional feelings are based on representations in the midbrain (2), which are further elaborated in cortical systems (3). However, how these computations relate to phenomenal experience in humans is largely unknown. Here, we show that a shallow convolutional neural network based on the Drosophila visual system predicts human behavioral and brain responses across development. In laboratory experiments using controlled visual stimuli, we find that this model explains defensive behaviors to looming objects in infants and superior colliculus responses to optical expansion in adults. Further, examining responses to a broader array of naturalistic video clips, we observe that representations of looming from this model predict self-reported emotion largely on the basis of subjective arousal. Our results illustrate how human emotions may be supported by species-general systems for survival in unpredictable environments. Cold Spring Harbor Laboratory 2023-08-31 /pmc/articles/PMC10491236/ /pubmed/37693448 http://dx.doi.org/10.1101/2023.08.29.555380 Text en https://creativecommons.org/licenses/by-nc/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Thieu, Monica K.
Ayzenberg, Vladislav
Lourenco, Stella F.
Kragel, Philip A.
Visual looming is a primitive for human emotion
title Visual looming is a primitive for human emotion
title_full Visual looming is a primitive for human emotion
title_fullStr Visual looming is a primitive for human emotion
title_full_unstemmed Visual looming is a primitive for human emotion
title_short Visual looming is a primitive for human emotion
title_sort visual looming is a primitive for human emotion
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10491236/
https://www.ncbi.nlm.nih.gov/pubmed/37693448
http://dx.doi.org/10.1101/2023.08.29.555380
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