Abstract
A gradual buildup of electrical potential over motor areas precedes self-initiated movements. Recently, such “readiness potentials” (RPs) were attributed to stochastic fluctuations in neural activity. We developed a new experimental paradigm that operationalized self-initiated actions as endogenous ‘skip’ responses while waiting for target stimuli in a perceptual decision task. We compared these to a block of trials where participants could not choose when to skip, but were instead instructed to skip. Frequency and timing of motor action were therefore balanced across blocks, so that conditions differed only in how the timing of skip decisions was generated. We reasoned that across-trial variability of EEG could carry as much information about the source of skip decisions as the mean RP. EEG variability decreased more markedly prior to self-initiated compared to externally-triggered skip actions. This convergence suggests a consistent preparatory process prior to self-initiated action. A leaky stochastic accumulator model could reproduce this convergence given the additional assumption of a systematic decrease in input noise prior to self-initiated actions. Our results may provide a novel neurophysiological perspective on the topical debate regarding whether self-initiated actions arise from a deterministic neurocognitive process, or from neural stochasticity. We suggest that the key precursor of self-initiated action may manifest as a reduction in neural noise.
Highlights
Functional and neuroanatomical evidence has been used to distinguish between two broad classes of human actions: self-initiated actions that happen endogenously, in the absence of any specific stimulus (Haggard, 2008; Passingham et al, 2010), and reactions to external cues
The capacity for endogenous voluntary action lies at the heart of human nature, but the brain mechanisms that enable this capacity remain unclear
Many existing paradigms rely on paradoxical instructions equivalent to “be voluntary”
Summary
Functional and neuroanatomical evidence has been used to distinguish between two broad classes of human actions: self-initiated actions that happen endogenously, in the absence of any specific stimulus (Haggard, 2008; Passingham et al, 2010), and reactions to external cues. The time of crossing a threshold for movement could depend in part on stochastic fluctuations in neural activity (Murakami et al, 2014; Schurger et al, 2012) Averaging such fluctuations time-locked to action initiation reproduced the “build-up” pattern of the mean RP, suggesting that the classical interpretation of RP as a stable precursor of voluntary action could be deceptive. On this account, RP is not a specific, goal-directed process that triggers action, but is rather an artefact of biased sampling and averaging of neural noise (Murakami et al, 2014; Schurger et al, 2012). We used a systematic modelling approach to show that a stochastic accumulator framework could explain the pattern of EEG variability, but only by assuming an additional process modulating the level of neural noise
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