Pinning down response inhibition in the brain — Conjunction analyses of the Stop-signal task

Abstract

Successful behavior requires a finely-tuned interplay of initiating and inhibiting motor programs to react effectively to constantly changing environmental demands. One particularly useful paradigm for investigating inhibitory motor control is the Stop-signal task, where already-initiated responses to Gostimuli are to be inhibited upon the rapid subsequent presentation of a Stop-stimulus (yielding successful and unsuccessful Stop-trials). Despite the extensive use of this paradigm in functional neuroimaging, there is no consensus on which functional comparison to use to characterize response-inhibition-related brain activity. Here, we utilize conjunction analyses of successful and unsuccessful Stop-trials that are each contrasted against a reference condition. This conjunction approach identifies processes common to both Stop-trial types while excluding processes specific to either, thereby capitalizing on the presence of some response-inhibition-related activity in both conditions. Using this approach on fMRI data from human subjects, we identify a network of brain structures that was linked to both types of Stop-trials, including lateral-inferior frontal and medial frontal cortical areas and the caudate nucleus. In addition, comparisons with a reference condition matched for visual stimulation identified additional activity in the right inferior parietal cortex that may play a role in enhancing the processing of the Stop-stimuli. Finally, differences in stopping efficacy across subjects were associated with variations in activity in the left anterior insula. However, this region was also associated with general task accuracy (which furthermore correlated directly with stopping efficacy), suggesting that it might actually reflect a more general mechanism of performance control that supports response inhibition in a relatively nonspecific way.

The role of the right presupplementary motor area in stopping action: two studies with event-related transcranial magnetic stimulation

“…The coordinate for the right preSMA (x ϭ 10, y ϭ 6, z ϭ 72) in Montreal Neurological Institute (MNI) space was determined from the group contrast of "critical Go-noncritical Go" from a previous fMRI study (Jahfari et al 2009) and this MNI coordinate was registered to individual structural space (FLIRT, FMRIB, Oxford, UK) (Jenkinson and Smith 2001). Another reason to target the right preSMA rather than the left preSMA (as was done in Chen et al 2009) is that many fMRI studies have reported the peak stopping-related activation of the preSMA in the right hemisphere (Aron and Poldrack 2006;Aron et al 2007a;Boecker et al 2010Boecker et al , 2011Boehler et al 2010;Cai and Leung 2009;Chao et al 2009;Chikazoe et al 2009b) and many studies point to a right-hemisphere white-matter network between the preSMA, the right IFG, and the basal ganglia (Aron et al 2007a;Forstmann et al 2012;King et al 2011;Madsen et al 2010;Swann et al 2012). Therefore, we consider that the right preSMA is probably a more representative region for stopping than the left preSMA.…”

“…The standard (nonselective) form of stopping is putatively implemented via the hyperdirect pathway to the subthalamic nucleus of the basal ganglia (Aron et al 2007b;Forstmann et al 2012;Jahfari et al 2011;Ray et al 2012), whereas the selective stopping could be implemented by the indirect pathway through the striatum. Although much evidence shows that the basic form of stopping recruits preSMA, right IFG, and the basal ganglia (Aron and Poldrack 2006;Boehler et al 2010;Leung 2009, 2011;Chevrier et al 2007;Chikazoe et al 2009b;Curtis et al 2005;Konishi et al 1999;Leung and Cai 2007;Li et al 2006;Rubia et al 2001;Vink et al 2005;Xue et al 2008) and a white-matter network connecting these nodes (Aron et al 2007a;Forstmann et al 2012;King et al 2011;Madsen et al 2010), the neural substrates of selective stopping are not well established, with just one study to date showing activation of the preSMA and right IFG (see Coxon et al 2009). …”

“…For example, the region that is critical for stopping might not overlap with the region that is critical for setting up the stopping rule and/or the one for modulating response tendencies. Indeed, fMRI studies do point to different loci in left/right anterior/posterior preSMA for different aspects of stopping, switching, and wider action control (Aron and Poldrack 2006;Boecker et al 2010;Boehler et al 2010;Brass and von Cramon 2002;Cai and Leung 2009;Chikazoe et al 2009a,b;Cunnington et al 2006;Dove et al 2000;Fassbender et al 2009;Leung and Cai 2007;Li et al 2006;Luks et al 2002Luks et al , 2007Rubia et al 2001;Rushworth et al 2002). Thus we might have affected the preSMA region for stopping (or for the stopping network) but missed the preSMA region critical for setting up the stopping rule and/or modulating response tendencies.…”

“…In functional magnetic resonance imaging (fMRI) studies, activation in the right preSMA (and usually also the anterior cingulate) is greater on trials for which participants successfully cancel a prepotent response compared with trials for which they do not (Aron and Poldrack 2006;Aron et al 2007a;Boecker et al 2010;Boehler et al 2010;Cai and Leung 2009;Chevrier et al 2007;Chikazoe et al 2009b;Curtis et al 2005;Hampshire et al 2010;Sharp et al 2010). Neurophysiologic studies have also shown activation in the preSMA prior to and during stopping (Chen et al 2010;Swann et al 2012).…”

Mapping the structure of perceptual and visual–motor abilities in healthy young adults

“…Therefore, the current task can only be considered in terms of overall achievement, and does not provide a measure of response inhibition failure, an important facet of response control (Boehler, Appelbaum, Krebs, Hopf, & Woldorff, 2010).…”