Neural signatures of vigilance decrements predict behavioural errors before they occur
- Macquarie University, Australia
- University of Cambridge, United Kingdom
Abstract
There are many monitoring environments, such as railway control, in which lapses of attention can have tragic consequences. Problematically, sustained monitoring for rare targets is difficult, with more misses and longer reaction times over time. What changes in the brain underpin these 'vigilance decrements'? We designed a multiple-object monitoring (MOM) paradigm to examine how the neural representation of information varied with target frequency and time performing the task. Behavioural performance decreased over time for the rare target (monitoring) condition, but not for a frequent target (active) condition. This was mirrored in neural decoding using Magnetoencephalography: coding of critical information declined more during monitoring versus active conditions along the experiment. We developed new analyses that can predict behavioural errors from the neural data more than a second before they occurred. This facilitates pre-empting behavioural errors due to lapses in attention and provides new insight into the neural correlates of vigilance decrements.
Data availability
We have shared the Magnetoencephalography data (i.e. time series) as well as behavioral data in Matlab '.mat' format on the Open Science Framework website at https://osf.io/5aw8v/ with the DOI: 10.17605/OSF.IO/5AW8V. We have also uploaded a video of the "Multiple-Object-Monitoring" paradigm, developed for this study, for easier understanding of the task at the same address. The mentioned address is dedicated to this project and we will regularly update the contents to make them easier to follow for other researchers.
-
Neural signatures of vigilance decrements predict behavioural errors before they occurOpen Science Framework, DOI 10.17605/OSF.IO/5AW8V.
Article and author information
Author details
Hamid Karimi-Rouzbahani
Funding
Australian Research Council (DP170101780)
- Anina N Rich
Australian Research Council (FT170100105)
- Alexandra Woolgar
MRC Cognition and Brain Sciences Unit (SUAG/052/G101400)
- Alexandra Woolgar
The Royal Society (NIF\R1\192608)
- Hamid Karimi-Rouzbahani
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: The Human Research Ethics Committee of Macquarie University approved the experimental protocols and the participants gave informed consent before participating in the experiment. The approval identifier is 52020297914411.
Reviewing Editor
- Peter Kok, University College London, United Kingdom
Version history
- Received: July 3, 2020
- Accepted: April 2, 2021
- Accepted Manuscript published: April 8, 2021 (version 1)
- Version of Record published: April 21, 2021 (version 2)
- Version of Record updated: August 8, 2023 (version 3)
Copyright
© 2021, Karimi-Rouzbahani et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,255
- Page views
-
- 152
- Downloads
-
- 5
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Neural signatures of vigilance decrements predict behavioural errors before they occur
eLife 10:e60563.
https://doi.org/10.7554/eLife.60563
Further reading
-
- Neuroscience
Perceptual decisions about sensory input are influenced by fluctuations in ongoing neural activity, most prominently driven by attention and neuromodulator systems. It is currently unknown if neuromodulator activity and attention differentially modulate perceptual decision-making and/or whether neuromodulatory systems in fact control attentional processes. To investigate the effects of two distinct neuromodulatory systems and spatial attention on perceptual decisions, we pharmacologically elevated cholinergic (through donepezil) and catecholaminergic (through atomoxetine) levels in humans performing a visuo-spatial attention task, while we measured electroencephalography (EEG). Both attention and catecholaminergic enhancement improved decision-making at the behavioral and algorithmic level, as reflected in increased perceptual sensitivity and the modulation of the drift rate parameter derived from drift diffusion modeling. Univariate analyses of EEG data time-locked to the attentional cue, the target stimulus, and the motor response further revealed that attention and catecholaminergic enhancement both modulated pre-stimulus cortical excitability, cue- and stimulus-evoked sensory activity, as well as parietal evidence accumulation signals. Interestingly, we observed both similar, unique, and interactive effects of attention and catecholaminergic neuromodulation on these behavioral, algorithmic, and neural markers of the decision-making process. Thereby, this study reveals an intricate relationship between attentional and catecholaminergic systems and advances our understanding about how these systems jointly shape various stages of perceptual decision-making.
