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Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection

Evidence accumulation models provide a dominant account of human decision-making, and have been particularly successful at explaining behavioral and neural data in laboratory paradigms using abstract, stationary stimuli. It has been proposed, but with limited in-depth investigation so far, that simi...

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Autores principales: Markkula, Gustav, Uludağ, Zeynep, Wilkie, Richard McGilchrist, Billington, Jac
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8282001/
https://www.ncbi.nlm.nih.gov/pubmed/34264935
http://dx.doi.org/10.1371/journal.pcbi.1009096
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author Markkula, Gustav
Uludağ, Zeynep
Wilkie, Richard McGilchrist
Billington, Jac
author_facet Markkula, Gustav
Uludağ, Zeynep
Wilkie, Richard McGilchrist
Billington, Jac
author_sort Markkula, Gustav
collection PubMed
description Evidence accumulation models provide a dominant account of human decision-making, and have been particularly successful at explaining behavioral and neural data in laboratory paradigms using abstract, stationary stimuli. It has been proposed, but with limited in-depth investigation so far, that similar decision-making mechanisms are involved in tasks of a more embodied nature, such as movement and locomotion, by directly accumulating externally measurable sensory quantities of which the precise, typically continuously time-varying, magnitudes are important for successful behavior. Here, we leverage collision threat detection as a task which is ecologically relevant in this sense, but which can also be rigorously observed and modelled in a laboratory setting. Conventionally, it is assumed that humans are limited in this task by a perceptual threshold on the optical expansion rate–the visual looming–of the obstacle. Using concurrent recordings of EEG and behavioral responses, we disprove this conventional assumption, and instead provide strong evidence that humans detect collision threats by accumulating the continuously time-varying visual looming signal. Generalizing existing accumulator model assumptions from stationary to time-varying sensory evidence, we show that our model accounts for previously unexplained empirical observations and full distributions of detection response. We replicate a pre-response centroparietal positivity (CPP) in scalp potentials, which has previously been found to correlate with accumulated decision evidence. In contrast with these existing findings, we show that our model is capable of predicting the onset of the CPP signature rather than its buildup, suggesting that neural evidence accumulation is implemented differently, possibly in distinct brain regions, in collision detection compared to previously studied paradigms.
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spelling pubmed-82820012021-07-28 Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection Markkula, Gustav Uludağ, Zeynep Wilkie, Richard McGilchrist Billington, Jac PLoS Comput Biol Research Article Evidence accumulation models provide a dominant account of human decision-making, and have been particularly successful at explaining behavioral and neural data in laboratory paradigms using abstract, stationary stimuli. It has been proposed, but with limited in-depth investigation so far, that similar decision-making mechanisms are involved in tasks of a more embodied nature, such as movement and locomotion, by directly accumulating externally measurable sensory quantities of which the precise, typically continuously time-varying, magnitudes are important for successful behavior. Here, we leverage collision threat detection as a task which is ecologically relevant in this sense, but which can also be rigorously observed and modelled in a laboratory setting. Conventionally, it is assumed that humans are limited in this task by a perceptual threshold on the optical expansion rate–the visual looming–of the obstacle. Using concurrent recordings of EEG and behavioral responses, we disprove this conventional assumption, and instead provide strong evidence that humans detect collision threats by accumulating the continuously time-varying visual looming signal. Generalizing existing accumulator model assumptions from stationary to time-varying sensory evidence, we show that our model accounts for previously unexplained empirical observations and full distributions of detection response. We replicate a pre-response centroparietal positivity (CPP) in scalp potentials, which has previously been found to correlate with accumulated decision evidence. In contrast with these existing findings, we show that our model is capable of predicting the onset of the CPP signature rather than its buildup, suggesting that neural evidence accumulation is implemented differently, possibly in distinct brain regions, in collision detection compared to previously studied paradigms. Public Library of Science 2021-07-15 /pmc/articles/PMC8282001/ /pubmed/34264935 http://dx.doi.org/10.1371/journal.pcbi.1009096 Text en © 2021 Markkula et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Markkula, Gustav
Uludağ, Zeynep
Wilkie, Richard McGilchrist
Billington, Jac
Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection
title Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection
title_full Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection
title_fullStr Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection
title_full_unstemmed Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection
title_short Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection
title_sort accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8282001/
https://www.ncbi.nlm.nih.gov/pubmed/34264935
http://dx.doi.org/10.1371/journal.pcbi.1009096
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