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 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.

[1]  P. Haggard,et al.  On the relation between brain potentials and the awareness of voluntary movements , 1999, Experimental Brain Research.

[2]  P. Haggard.  Human volition: towards a neuroscience of will , 2008, Nature Reviews Neuroscience.

[3]  Jonathan D. Cohen,et al.  The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. , 2006, Psychological review.

[4]  Xiao-Jing Wang.  Decision Making in Recurrent Neuronal Circuits , 2008, Neuron.

[5]  Fell Gs,et al.  Estimation and interpretation on plasma zinc fractions. , 1976 .

[6]  A. Pouget,et al.  Variance as a Signature of Neural Computations during Decision Making , 2011, Neuron.

[7]  C. Gallistel,et al.  Non-verbal numerical cognition: from reals to integers , 2000, Trends in Cognitive Sciences.

[8]  R. Ratcliff,et al.  Estimation and interpretation of 1/fα noise in human cognition , 2004 .

[9]  M. Hallett,et al.  What is the Bereitschaftspotential? , 2006, Clinical Neurophysiology.

[10]  Stanislas Dehaene,et al.  An accumulator model for spontaneous neural activity prior to self-initiated movement , 2012, Proceedings of the National Academy of Sciences.

[11]  J. Eccles.  Mental summation: The timing of voluntary intentions by cortical activity , 1985, Behavioral and Brain Sciences.

[12]  John C. Eccles,et al.  The initiation of voluntary movements by the supplementary motor area , 2004, Archiv für Psychiatrie und Nervenkrankheiten.

[13]  James L. McClelland,et al.  The time course of perceptual choice: the leaky, competing accumulator model. , 2001, Psychological review.

[14]  R. Passingham.  The frontal lobes and voluntary action , 1993 .

[15]  B. Libet,et al.  Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. , 1983 .

[16]  H. Kornhuber,et al.  Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale , 1965, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[17]  Benjamin Blankertz,et al.  The point of no return in vetoing self-initiated movements , 2015, Proceedings of the National Academy of Sciences.

[18]  D. Cheyne,et al.  Three-dimensional localization of SMA activity preceding voluntary movement , 2004, Experimental Brain Research.

[19]  K. R. Ridderinkhof,et al.  Striatum and pre-SMA facilitate decision-making under time pressure , 2008, Proceedings of the National Academy of Sciences.

[20]  Aaron Schurger,et al.  Specific Relationship between the Shape of the Readiness Potential, Subjective Decision Time, and Waiting Time Predicted by an Accumulator Model with Temporally Autocorrelated Input Noise , 2018, eNeuro.

[21]  Biyu J. He,et al.  Volition and Action in the Human Brain: Processes, Pathologies, and Reasons , 2017, The Journal of Neuroscience.

[22]  Patrick Haggard,et al.  Dissociating cognitive and motoric precursors of human self-initiated action , 2018, bioRxiv.

[23]  B. Libet,et al.  Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. , 1983, Brain : a journal of neurology.

[24]  B. Love,et al.  Measures of Neural Similarity , 2018, Computational Brain & Behavior.

[25]  C. Woody.  Characterization of an adaptive filter for the analysis of variable latency neuroelectric signals , 1967, Medical and biological engineering.

[26]  B. Libet.  Unconscious cerebral initiative and the role of conscious will in voluntary action , 1985, Behavioral and Brain Sciences.

[27]  Martin Luessi,et al.  MEG and EEG data analysis with MNE-Python , 2013, Front. Neuroinform..

[28]  Haym Hirsh,et al.  Learning to Predict Rare Events in Event Sequences , 1998, KDD.

[29]  T. Mima,et al.  Human presupplementary motor area is active before voluntary movement: subdural recording of Bereitschaftspotential from medial frontal cortex , 2000, Experimental Brain Research.

[30]  R. Bogacz,et al.  The neural basis of the speed–accuracy tradeoff , 2010, Trends in Neurosciences.

[31]  Margaret T. Lynn,et al.  Imaging volition: what the brain can tell us about the will , 2013, Experimental Brain Research.

[32]  Patrick Haggard,et al.  Precursor processes of human self-initiated action , 2017, NeuroImage.

[33]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.