Having a goal to stop action is associated with advance control of specific motor representations

Abstract

An important aspect of cognitive control consists in the ability to stop oneself from making inappropriate responses. In an earlier study we demonstrated that there are different mechanisms for stopping: global and selective [Aron, A. R., Verbruggen, F. (2008). Stop the presses: Dissociating a selective from a global mechanism for stopping. Psychological Science, 19(11) 1146–1153]. We argued that participants are more likely to use a global mechanism when speed is of the essence, whereas they are more likely to use a selective mechanism when they have foreknowledge of which response tendency they may need to stop. Here we further investigate the relationship between foreknowledge and selective stopping. In Experiment 1 we adapted the earlier design to show that individual differences in recall accuracy for the stopping goal correlate with the selectivity of the stopping. This confirms that encoding and using a foreknowledge memory cue is a key enabler for a selective stopping mechanism. In Experiment 2, we used transcranial magnetic stimulation (TMS), to test the hypothesis that foreknowledge “sets up” a control set whereby control is applied onto the response representation that may need to be stopped in the future. We applied TMS to the left motor cortex and measured motor evoked potentials (MEPs) from the right hand while participants performed a similar behavioral paradigm as Experiment 1. In the foreknowledge period, MEPs were significantly reduced for trials where the right hand was the one that might need to be stopped relative to when it was not. This shows that having a goal of what response may need to be stopped in the future consists in applying advance control onto a specific motor representation.

Introduction

Much human cognitive control consists in the ability to stop inappropriate action. In real-world scenarios such control is usually proactive in the sense that people have goals (or foreknowledge) of what they need to stop even if they are not currently trying to stop any impulse or action. Here we explore the neurocognitive basis for how foreknowledge is used to stop particular response tendencies.

A good experimental paradigm for examining the stopping of an incipient response tendency is the stop-signal paradigm (reviewed by Verbruggen & Logan, 2009). In the standard paradigm, on each trial, the participant initiates a choice response, and then, on a minority of trials, must try to stop the initiated response when a stop signal occurs. The main dependent measure is the speed of the stopping process, stop-signal reaction time. In the standard version, the participant has a general goal to stop when a stop signal occurs, but he or she does not need to deploy this selectively for one motor representation rather than another. In such situations, a fast but ‘global’ mechanism is probably used to stop the response tendency. The mechanism is global in the sense that it has effects on muscle representations over and above the particular muscle that needs to be stopped (Badry et al., 2009, Coxon et al., 2006, Coxon et al., 2007, Leocani et al., 2000, Sohn et al., 2002). However, stopping may also be achieved by means of a selective mechanism—i.e. one that has specific effects on particular motor representations rather than many (or all) possible representations. We provided evidence for dissociable global and selective stopping mechanisms by developing a novel version of the stop-signal paradigm (Aron & Verbruggen, 2008). On each trial participants initiated a coupled response with fingers of both hands, and then, when a stop signal occurred, the participant tried to stop one response while continuing with the other one (see Fig. 1A and B). This design allows a measurement of the selectivity of the stopping in terms of the degree of interference that is produced in the alternative (non-stopped) response—we refer to this as the ‘stopping interference effect’. We compared a condition in which foreknowledge was provided of which response(s) may need to be stopped compared to a condition where no foreknowledge was provided. To do this, we presented the cues “Maybe Stop Left”, “Maybe Stop Right” and “Maybe Stop XXX” in the foreknowledge period. Our key finding was that the stopping interference effect was reduced whereas stop-signal reaction time was increased when foreknowledge was provided compared to when it was not. We argued that when foreknowledge is provided stopping is more selective precisely because the participant uses the stopping goal (foreknowledge) to prepare to stop a specific response tendency. We speculate that this type of selective stopping is slower because it involves a fronto-basal-ganglia circuit with more synapses than the one that is putatively used to stop quickly (and globally) (c.f. Aron and Verbruggen, 2008, Aron et al., 2007)—although this remains to be established empirically.

Here we investigate the neurocognitive mechanisms by which foreknowledge is used to stop particular response tendencies. For Experiment 1 we had two objectives: to replicate our earlier result that stopping is more selective (and slower) for a foreknowledge vs. no foreknowledge condition (Aron & Verbruggen, 2008); and to show that, across participants, those with better recall of the foreknowledge rule are those who are able to stop more selectively. This would help to establish an important link between working memory for stopping goals and the mechanism of inhibitory control that ostensibly underlies the behavioral stopping itself. To examine the relationship between foreknowledge and selective stopping a key addition was made to the design used in Aron and Verbruggen (2008). On a minority of stop-signal trials in the foreknowledge condition, the stop signal was uninformative about which response to stop, thus serving as a memory probe. On probe trials, the stop signal was presented at the center of the screen (Fig. 1C). When this ‘probe’ occurred the participant was required to stop the response that had been indicated by the foreknowledge cue. This design feature allowed us to compute ‘cue recall accuracy’—a measure of working memory for the foreknowledge cue. This accuracy measure reflected the proportion of probe trials when the participant correctly stopped the required hand out of all probe trials when they stopped one or both hands. We predicted that those participants with higher cue recall accuracy scores would be those with smaller stopping interference effects. This result would provide further evidence that knowledge of the stopping goal is a key enabler of selective stopping.

Experiment 2 tested a neurocognitive hypothesis about how foreknowledge enables selective stopping. We hypothesized that foreknowledge “sets up” a control set whereby control is applied onto the response representation that may need to be stopped in the future. This predicts that the motor representation of the response that might need to be stopped in the future is affected by the foreknowledge before the response is even initiated. Testing this idea requires a technique that can measure the state of specific motor representations with high temporal resolution. Here we used TMS of the primary motor cortex, using surface electromyography to record evoked potentials from intrinsic muscles of the hand. We delivered TMS stimuli to the left primary motor cortex at specific time-points in the foreknowledge period while participants performed a behavioral paradigm similar to Experiment 1, i.e. making coupled responses with little or index fingers of both hands, and trying to stop one hand when indicated, for both foreknowledge and no foreknowledge conditions. We recorded MEPs from the right first dorsal interosseous muscle (FDI). These MEPs provide a measure of corticomotor excitability for the index finger response representation. We predicted that when the cue was ‘Maybe Stop Right’ the MEP for the right index finger would be significantly reduced compared to when the cue was ‘Maybe Stop Left’. We expected that corticomotor excitability for the ‘Maybe Stop XXX’ condition would either be similar to ‘Maybe Stop Left’ (participants do not prepare to stop the right hand) or else intermediate between ‘Maybe Stop Left’ and ‘Maybe Stop Right’ (participants expect to stop the right hand to some extent). An alternative outcome was that there would be no effect of foreknowledge cue on MEPs in the foreknowledge period. This would indicate that preparing to stop happens at a purely cognitive level, without any effects on the motor system until stopping itself is needed.