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

Autor: Richard M. Wilkie, Zeynep Uludağ, Gustav Markkula, Jac Billington
Jazyk: angličtina
Rok vydání: 2021
Předmět:
Male
Time Factors
Computer science
Physiology
Vision
Social Sciences
Event-Related Potentials
02 engineering and technology
Electroencephalography
0302 clinical medicine
Cognition
0203 mechanical engineering
Looming
Task Performance and Analysis
0202 electrical engineering
electronic engineering
information engineering

Medicine and Health Sciences
Psychology
Biology (General)
media_common
Clinical Neurophysiology
Brain Mapping
Ecology
medicine.diagnostic_test
05 social sciences
Brain
Replicate
Middle Aged
Electrophysiology
020303 mechanical engineering & transports
Bioassays and Physiological Analysis
Computational Theory and Mathematics
Brain Electrophysiology
Modeling and Simulation
Physical Sciences
Sensory Perception
Female
Anatomy
Research Article
Adult
Imaging Techniques
QH301-705.5
020209 energy
media_common.quotation_subject
Decision Making
Models
Neurological

Neurophysiology
Sensory system
Neuroimaging
Research and Analysis Methods
050105 experimental psychology
03 medical and health sciences
Cellular and Molecular Neuroscience
Young Adult
Event-related potential
Perception
Genetics
medicine
Humans
0501 psychology and cognitive sciences
Collision detection
Molecular Biology
Ecology
Evolution
Behavior and Systematics

Behavior
Scalp
Electrophysiological Techniques
Cognitive Psychology
Biology and Life Sciences
Computational Biology
Collision
Probability Theory
Probability Distribution
Space Perception
Cognitive Science
Clinical Medicine
Neuroscience
Head
030217 neurology & neurosurgery
Mathematics
Zdroj: PLoS Computational Biology, Vol 17, Iss 7, p e1009096 (2021)
PLoS Computational Biology
ISSN: 1553-7358
1553-734X
Popis: 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.
Databáze: OpenAIRE
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