Many studies have shown that movements are preceded by early brain signals. There has been a debate as to whether subjects can still cancel a movement after onset of these early signals. We tested whether subjects can win a “duel” against a brain–computer interface designed to predict their movements in real time from observations of their EEG activity. Our findings suggest that subjects can exert a “veto” even after onset of this preparatory process. However, the veto has to occur before a point of no return is reached after which participants cannot avoid moving.

In humans, spontaneous movements are often preceded by early brain signals. One such signal is the readiness potential (RP) that gradually arises within the last second preceding a movement. An important question is whether people are able to cancel movements after the elicitation of such RPs, and if so until which point in time. Here, subjects played a game where they tried to press a button to earn points in a challenge with a brain–computer interface (BCI) that had been trained to detect their RPs in real time and to emit stop signals. Our data suggest that subjects can still veto a movement even after the onset of the RP. Cancellation of movements was possible if stop signals occurred earlier than 200 ms before movement onset, thus constituting a point of no return.

It has been repeatedly shown that spontaneous movements are preceded by early brain signals (1⇓⇓⇓⇓⇓⇓–8). As early as a second before a simple voluntary movement, a so-called readiness potential (RP) is observed over motor-related brain regions (1⇓–3, 5). The RP was found to precede the self-reported time of the “‘decision’ to act” (ref. 3, p. 623). Similar preparatory signals have been observed using invasive electrophysiology (8, 9) and functional MRI (7, 10), and have been demonstrated also for choices between multiple-response options (6, 7, 10), for abstract decisions (10), for perceptual choices (11), and for value-based decisions (12). To date, the exact nature and causal role of such early signals in decision making is debated (12⇓⇓⇓⇓⇓⇓⇓–20).

One important question is whether a person can still exert a veto by inhibiting the movement after onset of the RP (13, 18, 21, 22). One possibility is that the onset of the RP triggers a causal chain of events that unfolds in time and cannot be cancelled. The onset of the RP in this case would be akin to tipping the first stone in a row of dominoes. If there is no chance of intervening, the dominoes will gradually fall one-by-one until the last one is reached. This has been coined a ballistic stage of processing (23, 24). A different possibility is that participants can still terminate the process, akin to taking out a domino at some later stage in the chain and thus preventing the process from completing. Here, we directly tested this in a real-time experiment that required subjects to terminate their decision to move once a RP had been detected by a brain–computer interface (BCI) (25⇓⇓⇓⇓⇓–31).

Results

Subjects were confronted with a floor-mounted button and a light presented on a computer screen. Once the light turned green (“go signal”), subjects waited for a short, self-paced period of about 2 s after which they were allowed to press the button with their right foot at any time. They could earn points if they pressed while the light was green, but lose points if they pressed after the light had turned red (“stop signal”). The experiment had three consecutive stages (Fig. 1A). In stage I, stop signals were elicited at random onset times (sampled from a uniform distribution); thus, the movements were not being predicted. The EEG data from stage I were then used to train a classifier to predict upcoming movements in the next two stages of the experiment. In stage II, movement predictions were made in real time by the BCI with the aim of turning the stop signal on in time to interrupt the subject’s movement. The term “prediction” will be used here to denote any above-chance level of predictive accuracy, not only perfect prediction. After stage II, subjects were informed that they were being predicted by the computer and that they should try and move unpredictably, and another otherwise-identical stage followed.

Fig. 1. Experimental design and possible trial outcomes. (A) The experiment consisted of three consecutive stages. During stage I, the stop signals were random. After stage I, a classifier was trained on button presses from stage I and the BCI predictor was activated. In the subsequent stages II and III, stop signals were elicited in real time by the BCI predictor. After stage II, subjects were informed about the predictor and instructed to try and move unpredictably. (B) Possible trial outcomes (see main text).

The mean waiting time between trial start and electromyogram (EMG) onset across subjects and stages was 5,441 ms. The mean movement duration from EMG onset to button press across subjects and stages was 316 ms. There was no significant effect of stage on waiting time [F (2,18) = 3.36, P = 0.06], but a significant effect of stage on movement velocity [F (2,18) = 9.86, P = 0.0013], such that movements were faster in stages II and III (see SI Appendix, Fig. S1, for details on stages).

Fig. 2 shows average RPs, EMG signals, and button press times. During all of the experimental stages, the event-related potential time-locked to EMG onset showed the typical exponential-looking RP with a peak over channel Cz (2). The RP was not lateralized at any time, which is to be expected for foot movements (32) where the cortical motor representation is on the medial wall. Despite the differences in experimental conditions, there was no significant difference between RPs in the three stages (Fig. 2). Thus, the instruction given to subjects between stages II and III to use strategies to avoid prediction did not alter the shape of the RP. We further performed a qualitative assessment of the amplitude of the RP at EMG onset. For this, we used the cross-validated classifier output at EMG onset (for details see Experimental Procedures) as an estimate for RP amplitude, since both quantities are directly related. The amplitude of the RP at EMG onset showed a significant negative correlation both with waiting time (r = −0.10; P = 0.009) and with movement duration (r = −0.25; P < 0.001).

Fig. 2. Mean readiness potential (RP), EMG activity, and button press distribution. The top panel shows the average squared EMG potential recorded at the right calf, averaged over all stages and subjects. The Inset on the Right shows the button press distribution relative to EMG onset, pooled across stages and subjects. The three colored lines in the bottom panel show the grand average RP at channel Cz, during individual stages of the experiment. For stage I missed button press trials were used, for stages II and III silent trials were used because these were not interrupted by the BCI (see text for details on silent trials). Individual RPs were averaged across subjects (colored shadings indicate SEM). The scalp topographies show the EEG potential of all recorded channels, averaged over three time intervals indicated by the shaded regions: [−550 −400] ms, [−150 0] ms, and [250 400] ms. There was no significant difference between RPs of the three stages [F (2,18) = 0.02, P = 0.97; F (2,18) = 0.12, P = 0.89; and F (2,18) = 0.20, P = 0.82, respectively].

Each trial could end in one of four possible ways (Fig. 1B): In the first case, a subject would press the button while the light was green without a RP being detected. We refer to these as “missed button press” trials. In this case, the participant won. A second case was when the computer detected the RP, turned on the stop signal, and the subject subsequently pressed the button within the next 1,000 ms. We term this a “predicted button press” trial. In this case, the computer has won the trial. Another possibility is that the BCI indicated a RP and elicited a stop signal but the subject did not press the button within 1,000 ms. Here, neither the participant won (because they did not manage to press the button without being detected) nor the computer won (because the participant did not move as the task required). At first sight, one might consider all of these trials as false alarms where the classifier indicated a movement while the participant had neither made a decision nor initiated a movement. However, it is also possible that the classifier detected a movement that was being prepared but that the participant was able to cancel in time. One such case would be if the participant started to move (as indicated by the EMG) but then did not complete the button press. We term this an “aborted button press” trial. A different possibility is that the stop signal was elicited but the participant showed no overt sign of movement. This could either result from a prepared movement being terminated at an early stage, which we call an “early cancellation.” Alternatively, this could reflect spurious or false-positive detection by the classifier, which we term a proper “false alarm.” As there is no observable difference between these latter two cases, we jointly refer to them as “ambiguous” or “early cancellation/false alarm” trials. Fig. 3 shows the proportion of trials that had these four outcomes, separately for stages I, II, and III:

i) Missed button presses: In stage I (black bars in Fig. 3) when stop signals were random, most trials (66.5%) end with an undetected button press, i.e., the subject wins. The proportion of these trials is substantially reduced in stages II and III when the classifier is active [31.9% and 30.8%, respectively; paired t (9) = 6.49, P < 0.001, and paired t (9) = 9.99, P < 0.001]. There is no difference in the number of undetected button press trials between stages II and III despite the fact that subjects were informed of being predicted and they were instructed to act unpredictably before stage III [paired t (9) = 0.33, P = 0.75].

ii) Predicted button presses: In stage I, a very small number of trials (1.2%) ends with a detected button press, i.e., a case where the (random) “classifier” has won. In contrast, during stages II and III, the proportion of such trials is strongly increased by a factor of around 18 [19.5% and 22.8%; paired t (9) = 5.52, P < 0.001, and paired t (9) = 7.19, P < 0.001].

iii) Aborted button presses: In stage I, aborted button presses occur very rarely (2.2%), a rate that substantially increased in stages II and III [15.2% and 16.3%; paired t (9) = 2.67, P = 0.025, and paired t (9) = 2.81, P = 0.020].

iv) Ambiguous (early cancellations or false alarms): These types of trials occurred with similar rates in stages I, II, and III (30.1%, 33.5%, and 30.0%) with no significant difference between stage I and stages II and III [paired t (9) = 0.77, P = 0.46, and paired t (9) = 0.023, P = 0.98].

Fig. 3. Percentage of trial outcomes across stages for the four trial categories (as in Fig. 1B). All trial categories in one stage (bars of same color) add up to 100%. Shown is the average across subjects (error bars indicate SEM).

If one were to count any movement after a stop signal (whether completed or aborted) as a win for the BCI predictor, then the proportion of trials on which the BCI wins is considerably increased and there is no significant difference between subject wins and BCI wins in stages II and III [34.6% versus 39.1%; t (9) = −0.27, P = 0.79, and paired t (9) = −0.88, P = 0.39].

We also assessed how the timing of stop signals was related to movement onsets (as assessed by EMG). Fig. 4A (red) shows the distribution of stop signals in predicted button press trials. The vast majority of stop signals occurred after EMG onset; thus, when subjects had already begun to move but before the button was depressed. Here, the stop signal presumably came too late to prevent the subjects from finishing their movement and pressing the button. Fig. 4B (green) shows the distribution of stop signal times for aborted button press trials. Here, the stop signals occurred earlier (starting around 200 ms before EMG). Thus, when stop signals were presented at late stages of movement preparation subjects could not prevent beginning to move, even though they could abort the movement. There was a gradual transition between stop signal times where movements could be aborted and those where they could not be aborted (Fig. 4C). This presumably reflects a variability in trial-by-trial stop signal reaction times (24).

Fig. 4. Distribution of BCI predictions time-locked to EMG onset (vertical line). The three panels show the distribution of stop signals timings in predicted button press trials (A, red) and in aborted button press trials (B, green). C (red and green) shows their joint distribution. The black distribution superimposed as outline in all three panels shows the stop signal distribution in silent trials adjusted to account for the imbalanced probability of a trial being silent (40%) or not (60%). All bins comprised intervals of 100 ms, and counts were pooled across stages II and III of all subjects. Please note that, in silent trials, the distributions refer to the first stop signals that would have been emitted.

There were hardly any cases where subjects moved despite being presented with stop signals earlier than 200 ms before EMG. This is interesting given that the RP onset occurred more than 1,000 ms before EMG onset (Fig. 2). One possibility is that some detections were made at this early stage but that participants were almost always able to cancel the movement completely. To assess how early predictions could be made in principle, independent of the presentation of a stop signal, we studied the behavior of the predictor when stop signals were omitted. For this, 40% of trials in stages II and III were “silent trials”: Here, when the BCI predicted a movement, the time was silently recorded but the stop signal was not turned on and the trial continued until the button was pressed. As Fig. 4 A–C (black distribution) shows, a majority of predictions also in silent trials occurred around movement onset. However, many silent predictions occurred more than 200 ms before movement onset, compatible with the early RP onset. These early predictions were not found for predicted button press trials (Fig. 4A, red) or aborted button press trials (Fig. 4B, green) when stop signals are active. Thus, had the stop signal been active for these early predictions, subjects might have been caught preparing a movement but been able to cancel preparation early enough to prevent any observable movement. Resolving this issue would directly address the question of whether trials with stop signals, but no overt movements, constitute early cancellations or false alarms, and thus help interpret this ambiguous trial category.

If a proportion of these trials indeed reflected early cancellations instead of false alarms, one might observe some signs of movement preparation given that movement-predictive signals have been proposed to start before a decision (19). However, testing for the presence of an RP in the ambiguous trials would be biased: The classifier was trained to detect a RP and thus a false alarm should exhibit an RP-like topography as well. Thus, we searched for an independent indicator of movement preparation on ambiguous trials that was not based on the RP. For this we chose the event-related desynchronization (ERD) that occurs before and during movements in particular frequency bands in the EEG (33). ERD and RPs have been shown to have different generators in the brain and thus provide different information, therefore making ERD an index for motor preparation that is independent of the RP (34). We trained a classifier on the power contrast in those bands and tested it on the ambiguous trials (for full information on methods and results, see SI Appendix, Fig. S2). In this independent ERD analysis, movement preparation was also detected in ambiguous trials, but not in the random stop signal trials from stage I. Thus, at least a subset of ambiguous trials had likely already reached movement preparation and thus were not false alarms, but rather early cancellations.

We also used a questionnaire after each stage to assess subjects’ experiences and strategies during the different sections of the experiment (see SI Appendix, Supplemental Methods and Results, for details). When asked about their strategies during stages II and III, they reported “not thinking about the movements” (5 of 10), “pressing earlier” (4 of 10), or “trying to be more spontaneous” (4 of 10). When asked about whether they felt a connection between actions and the control of the light, several subjects reported that thinking about the movement caused the interruption (i.e., the light turning to red). As mentioned above, the changes revealed by the behavioral analyses did not result in a modification of the recorded RP.