A proactive mechanism for selective suppression of response tendencies

Abstract

While most research on stopping action examines how an initiated response is stopped when a signal occurs (i.e., reactively), everyday life also calls for a mechanism to prepare to stop a particular response tendency (i.e., proactively and selectively). We hypothesized that human subjects can prepare to stop a particular response by proactively suppressing that response representation in the brain. We tested this by using single-pulse transcranial magnetic stimulation and concurrent electromyography. This allowed us to interrogate the corticomotor excitability of specific response representations even before action ensued. We found that the motor evoked potential of the effector that might need to be stopped in the future was significantly reduced compared with when that effector was at rest. Further, this neural index of proactive and selective suppression predicted the subsequent selectivity with which the behavioral response was stopped. These results go further than earlier reports of reduced motor excitability when responses are stopped. They show that the control can be applied in advance (proactively) and also targeted at a particular response channel (selectively). This provides novel evidence for an active mechanism of suppression in the brain that is setup according to the subject's goals and even before action ensues.

Figure 1.

a, The selective stopping paradigm. Trials are shown for MSR and null conditions. A cue was followed by a delay and then the go signal—a row of four circles. If the two outer circles were blue, two responses were simultaneously initiated with little fingers of each hand; if the inner circles were blue, then index fingers were used. On probe trials a red “X” occurred soon after the go signal, requiring stopping of one response and continuing the other. On null trials the subject rested. b, A single TMS stimulus was delivered over left primary motor cortex. MEPs were recorded from the right hand. c, Hypothetical MEP results for the suppression and facilitation models.

Figure 2.

a, Preparing to stop the right hand (MSR) leads to suppression of right hand excitability beneath baseline (null) even before the response is initiated (Note: this analysis includes all trials regardless of whether they are subsequently go or stop.) b, The MEP results match the suppression model in Figure 1c. MEP data are shown for the 500 ms time point alone—see dotted rectangle in a. c, Relation between neural suppression and behavioral stopping. When preparing to stop the right hand, the MEP suppression of that hand (MSR minus null) correlates with the subsequent selectivity of stopping (the stopping interference effect). d, When preparing to stop the left hand, the MEP suppression of the right hand (MSL minus null) does not correlate with the stopping interference. The observations in c and d reflect successful stop trials only, and these are pooled across all subjects. The stopping interference effect is the probe alternative RT minus the mean of the go alternative RT for that subject. The neural measure is the size of the MEP on that trial minus the mean of the MEPs for null trials at the corresponding time point (800, 500, and 200) for that subject. Error bars show SD; *p < 0.01.

Figure 3.

A schematic model of how proactive and selective suppression is set up and used for behaviorally selective stopping. In the proactive and selective control stage, the stopping goal “Maybe Stop Right” biases particular response channels (right hand) without affecting the execution level. In the response initiation stage, the go signal initiates two responses (left and right index fingers). In the reactive and selective stopping stage, the stop signal triggers the selective suppression mechanism that was set up previously, thus stopping the right index finger but not the left index finger.