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.