One action system or two? Evidence for common central preparatory mechanisms in voluntary and stimulus-driven actions

Abstract

Human behavior is comprised of an interaction between intentionally driven actions and reactions to changes in the environment. Existing data are equivocal concerning the question of whether these two action systems are independent, involve different brain regions, or overlap. To address this question we investigated whether the degree to which the voluntary action system is activated at the time of stimulus onset predicts reaction times to external stimuli. We recorded event-related potentials while participants prepared and executed left- or right-hand voluntary actions, which were occasionally interrupted by a stimulus requiring either a left- or right-hand response. In trials where participants successfully performed the stimulus-driven response, increased voluntary motor preparation was associated with faster responses on congruent trials (where participants were preparing a voluntary action with the same hand that was then required by the target stimulus), and slower responses on incongruent trials. This suggests that early hand-specific activity in medial frontal cortex for voluntary action trials can be used by the stimulus-driven system to speed responding. This finding questions the clear distinction between voluntary and stimulus-driven action systems.

Figure 1.

Trial sequence for voluntary action trials (A) and target trials (B). ITI, Intertrial interval; SOA, stimulus onset asynchrony.

Figure 2.

RT distributions in 25 ms time windows from 0 to 1000 ms for congruent (A), and incongruent (B) responses averaged across all participants. Values on the y-axis correspond to the proportion of trials falling in each RT bin, with the x-axis representing RT. The vertical line represents the mean RT cutoff for separating the two distributions.

Figure 3.

Motor activation before action onset for voluntary action trials (A, B) and stimulus onset for target trials (C, D). A, B, RP (A) and LRP (B) onset before action onset for voluntary action trials. C, D, RP (C) and LRP (D) before S2 onset (0 ms) for target trials: Gray lines signify trials where the voluntary action was performed (as identified by individual participant RT distribution), and black lines indicate trials where participants genuinely responded to the target stimulus. Solid lines indicate trials where the S2 stimulus was congruent with the intended voluntary action, and dashed lines indicate incongruent trials. LRP plotted relative to the correct response to the target stimulus, such that negative values correspond to activation of the hand required by the target stimulus. E–J, Topographic plots show ERP amplitude averaged over the 500 ms period before action/stimulus onset for left-hand (E–G) and right-hand actions (H–J), for voluntary actions on voluntary action trials (E, H) and on target trials (F, I) as well as for target responses (G, J).

Figure 4.

RT dependent on prestimulus RP and LRP for congruent (A) and incongruent (B) trials separately. Error bars show standard error.