Proactive Selective Response Suppression Is Implemented via the Basal Ganglia

Abstract

In the welter of everyday life, people can stop particular response tendencies without affecting others. A key requirement for such selective suppression is that subjects know in advance which responses need stopping. We hypothesized that proactively setting up and implementing selective suppression relies on the basal ganglia and, specifically, regions consistent with the inhibitory indirect pathway for which there is scant functional evidence in humans. Consistent with this hypothesis, we show, first, that the degree of proactive motor suppression when preparing to stop selectively (indexed by transcranial magnetic stimulation) corresponds to striatal, pallidal, and frontal activation (indexed by functional MRI). Second, we demonstrate that greater striatal activation at the time of selective stopping correlates with greater behavioral selectivity. Third, we show that people with striatal and pallidal volume reductions (those with premanifest Huntington's disease) have both absent proactive motor suppression and impaired behavioral selectivity when stopping. Thus, stopping goals are used to proactively set up specific basal ganglia channels that may then be triggered to implement selective suppression. By linking this suppression to the striatum and pallidum, these results provide compelling functional evidence in humans of the basal ganglia's inhibitory indirect pathway.

Proactive modulation of long-interval intracortical inhibition during response inhibition

“…This finding is consistent with functional magnetic resonance imaging studies showing a similar pattern of neural activation between the three Stop trial types (Coxon et al 2009(Coxon et al , 2012(Coxon et al , 2016. Conversely, functional imaging results from Majid et al (2013) suggest a distinct role of the selective indirect basal ganglia pathway during partial stopping. Activation of the indirect pathway should have no effect on MEP amplitude in the responding finger during Partial trials.…”

“…A likely explanation is that MEP amplitude reflects the net excitatory and inhibitory inputs whereas LICI provides a measure of inhibition only. How LICI is modulated within the proactive response inhibition network remains unclear (Majid et al 2013;Van Belle et al 2014). The present study supports the idea that proactive and reactive control mechanisms are not independent but rather reactive stopping depends on ongoing proactive control (Dunovan et al 2015).…”

“…Transcranial magnetic stimulation (TMS) has been used to assess the temporal modulation of corticomotor excitability (CME) during both types of response inhibition. Proactive stopping is suggested to recruit the indirect basal ganglia pathway to selectively decrease CME for only the movement cued to stop (Aron and Verbruggen 2008;Cai et al 2011;Majid et al 2013). A topic of current debate is whether reactive stopping can be achieved selectively (Xu et al 2015), given that several lines of evidence indicate a transient process in which stopping response preparation suppresses movement nonselectively.…”

Training voluntary motor suppression with real-time feedback of motor evoked potentials

“…For example, in one kind of proactive suppression paradigm, participants are cued that they might have to stop a particular muscle later in a trial. By implementing motor suppression well in advance, they are better able to stop action in a targeted way when needed (Cai et al 2011;Chikazoe et al 2009;Jahfari et al 2012;Majid et al 2013;Smittenaar et al 2013).…”

The anticue task: no effect of working memory load on inhibitory control

“…More precisely, for proactive selective response suppression, new research evidence has shown that the right inferior frontal cortex seems to interact with the striatum and pallidum (8). Therefore, this basal ganglia's inhibitory indirect pathway is proposed to be activated during the present anticue task.…”