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:	Gustav Markkula, Zeynep Uludağ, Richard McGilchrist Wilkie, Jac Billington
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/b8bae550f1f849b7b7d2cbd965e76533
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spelling	oai:doaj.org-article:b8bae550f1f849b7b7d2cbd965e765332021-12-02T19:57:32ZAccumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection.1553-734X1553-735810.1371/journal.pcbi.1009096https://doaj.org/article/b8bae550f1f849b7b7d2cbd965e765332021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009096https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Evidence 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.Gustav MarkkulaZeynep UludağRichard McGilchrist WilkieJac BillingtonPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 7, p e1009096 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Gustav Markkula Zeynep Uludağ Richard McGilchrist Wilkie Jac Billington Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection.
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.
format	article
author	Gustav Markkula Zeynep Uludağ Richard McGilchrist Wilkie Jac Billington
author_facet	Gustav Markkula Zeynep Uludağ Richard McGilchrist Wilkie Jac Billington
author_sort	Gustav Markkula
title	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_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_sort	accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/b8bae550f1f849b7b7d2cbd965e76533
work_keys_str_mv	AT gustavmarkkula accumulationofcontinuouslytimevaryingsensoryevidenceconstrainsneuralandbehavioralresponsesinhumancollisionthreatdetection AT zeynepuludag accumulationofcontinuouslytimevaryingsensoryevidenceconstrainsneuralandbehavioralresponsesinhumancollisionthreatdetection AT richardmcgilchristwilkie accumulationofcontinuouslytimevaryingsensoryevidenceconstrainsneuralandbehavioralresponsesinhumancollisionthreatdetection AT jacbillington accumulationofcontinuouslytimevaryingsensoryevidenceconstrainsneuralandbehavioralresponsesinhumancollisionthreatdetection
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Accumulation of continuously time-varying sensory evidence constrains neural and behavioral responses in human collision threat detection.

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