Do readiness potentials happen all the time?

The Readiness Potential (RP) is a slow negative EEG potential found in the seconds preceding voluntary actions. Here, we explore whether the RP is found only at this time, or if it also occurs when no action is produced. Recent theories suggest the RP reflects the average of accumulated stochastic f...

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Main Authors: Eoin Travers, Nima Khalighinejad, Aaron Schurger, Patrick Haggard
Format: Article
Language:English
Published: Elsevier 2020-02-01
Series:NeuroImage
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811919308778
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spelling doaj-1b6d27d9e4da4d9482668db399da84742020-11-25T03:02:24ZengElsevierNeuroImage1095-95722020-02-01206116286Do readiness potentials happen all the time?Eoin Travers0Nima Khalighinejad1Aaron Schurger2Patrick Haggard3Institute of Cognitive Neuroscience, University College London, UK; Corresponding author. Institute of Cognitive Neuroscience, University College London, London, WC1N 3AR, UK.Institute of Cognitive Neuroscience, University College London, UK; Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, UKINSERM U992, Cognitive Neuroimaging Unit, Gif sur Yvette, 91191, France; Commissariat à l’Energie Atomique, Direction des Sciences du Vivant, I2BM, NeuroSpin center, Gif sur Yvette, 91191, France; Department of Psychology, Crean College of Health and Behavioral Sciences, Chapman University, Orange, CA, USA; Institute for Interdisciplinary Brain and Behavioral Sciences, Chapman University, Irvine, CA, USAInstitute of Cognitive Neuroscience, University College London, UKThe Readiness Potential (RP) is a slow negative EEG potential found in the seconds preceding voluntary actions. Here, we explore whether the RP is found only at this time, or if it also occurs when no action is produced. Recent theories suggest the RP reflects the average of accumulated stochastic fluctuations in neural activity, rather than a specific signal related to self-initiated action: RP-like events should then be widely present, even in the absence of actions. We investigated this hypothesis by searching for RP-like events in background EEG of an appropriate dataset for which the action-locked EEG had previously been analysed to test other hypotheses [Khalighinejad, N., Brann, E., Dorgham, A., Haggard, P. Dissociating cognitive and motoric precursors of human self-initiated action. Journal of Cognitive Neuroscience. 2019, 1-14]. We used the actual mean RP as a template, and searched the entire epoch for similar neural signals, using similarity metrics that capture the temporal or spatial properties of the RP. Most EEG epochs contained a number of events that were similar to the true RP, but did not lead directly to any voluntary action. However, these RP-like events were equally common in epochs that eventually terminated in voluntary actions as in those where voluntary actions were not permitted. Events matching the temporal profile of the RP were also a poor match for the spatial profile, and vice versa. We conclude that these events are false positives, and do not reflect the same mechanism as the RP itself. Finally, applying the same template-search algorithm to simulated EEG data synthesized from different noise distributions showed that RP-like events will occur in any dataset containing the 1⁄f noise ubiquitous in EEG recordings. To summarise, we found no evidence of genuinely RP-like events at any time other than immediately prior to self-initiated actions. Our findings do not support a purely stochastic model of RP generation, and suggest that the RP may be a specific precursor of self-initiated voluntary actions.http://www.sciencedirect.com/science/article/pii/S1053811919308778
collection DOAJ
language English
format Article
sources DOAJ
author Eoin Travers
Nima Khalighinejad
Aaron Schurger
Patrick Haggard
spellingShingle Eoin Travers
Nima Khalighinejad
Aaron Schurger
Patrick Haggard
Do readiness potentials happen all the time?
NeuroImage
author_facet Eoin Travers
Nima Khalighinejad
Aaron Schurger
Patrick Haggard
author_sort Eoin Travers
title Do readiness potentials happen all the time?
title_short Do readiness potentials happen all the time?
title_full Do readiness potentials happen all the time?
title_fullStr Do readiness potentials happen all the time?
title_full_unstemmed Do readiness potentials happen all the time?
title_sort do readiness potentials happen all the time?
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2020-02-01
description The Readiness Potential (RP) is a slow negative EEG potential found in the seconds preceding voluntary actions. Here, we explore whether the RP is found only at this time, or if it also occurs when no action is produced. Recent theories suggest the RP reflects the average of accumulated stochastic fluctuations in neural activity, rather than a specific signal related to self-initiated action: RP-like events should then be widely present, even in the absence of actions. We investigated this hypothesis by searching for RP-like events in background EEG of an appropriate dataset for which the action-locked EEG had previously been analysed to test other hypotheses [Khalighinejad, N., Brann, E., Dorgham, A., Haggard, P. Dissociating cognitive and motoric precursors of human self-initiated action. Journal of Cognitive Neuroscience. 2019, 1-14]. We used the actual mean RP as a template, and searched the entire epoch for similar neural signals, using similarity metrics that capture the temporal or spatial properties of the RP. Most EEG epochs contained a number of events that were similar to the true RP, but did not lead directly to any voluntary action. However, these RP-like events were equally common in epochs that eventually terminated in voluntary actions as in those where voluntary actions were not permitted. Events matching the temporal profile of the RP were also a poor match for the spatial profile, and vice versa. We conclude that these events are false positives, and do not reflect the same mechanism as the RP itself. Finally, applying the same template-search algorithm to simulated EEG data synthesized from different noise distributions showed that RP-like events will occur in any dataset containing the 1⁄f noise ubiquitous in EEG recordings. To summarise, we found no evidence of genuinely RP-like events at any time other than immediately prior to self-initiated actions. Our findings do not support a purely stochastic model of RP generation, and suggest that the RP may be a specific precursor of self-initiated voluntary actions.
url http://www.sciencedirect.com/science/article/pii/S1053811919308778
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