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.
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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.
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.
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Neural signatures of vigilance decrements predict behavioural errors before they occur
eLife 10:e60563.
https://doi.org/10.7554/eLife.60563
Further reading
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- Neuroscience
Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.
