4.6 Article

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

Journal

PLOS COMPUTATIONAL BIOLOGY
Volume 17, Issue 7, Pages -

Publisher

PUBLIC LIBRARY SCIENCE
DOI: 10.1371/journal.pcbi.1009096

Keywords

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Funding

  1. Wellcome Trust/University of Leeds Institutional Strategic 549 Support Fund [204825/Z/16/Z]
  2. UK Engineering and Physical Sciences Research Council [EP/S005056/1]
  3. Leverhulme Trust [RF-2019-343\10]
  4. EPSRC [EP/S005056/1] Funding Source: UKRI

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Evidence accumulation models of decision-making propose that humans accumulate noisy sensory evidence over time up to a decision threshold. We demonstrate that this type of model can describe human behavior well not only in abstract, semi-static laboratory tasks, but also in a task that is relevant to human movement in the real world. Specifically, we show that a model directly accumulating the continuously time-varying visual looming (optical expansion) of an approaching obstacle explains full probability distributions of when humans can detect this collision threat. Using electroencephalography, we find indications that this type of evidence is accumulated differently in the brain compared to evidence accumulation in previously studied, more abstract tasks.
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. Author summary Evidence accumulation models of decision-making propose that humans accumulate noisy sensory evidence over time up to a decision threshold. We demonstrate that this type of model can describe human behavior well not only in abstract, semi-static laboratory tasks, but also in a task that is relevant to human movement in the real world. Specifically, we show that a model directly accumulating the continuously time-varying visual looming (optical expansion) of an approaching obstacle explains full probability distributions of when humans can detect this collision threat. Using electroencephalography, we find indications that this type of evidence is accumulated differently in the brain compared to evidence accumulation in previously studied, more abstract tasks. Our experimental paradigm, model, and findings open for wider application of this type of decision-making model to laboratory and real-world tasks with ecologically relevant, time-varying sensory evidence, and further studies into how such decisions are implemented neurally. There are also societal implications: In applied safety research and traffic accident litigation it is conventionally assumed that human collision detection is limited by a fixed perceptual threshold, an assumption that our results show to be highly inaccurate.

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