Error-specific medial cortical and subcortical activity during the stop signal task: A functional magnetic resonance imaging study

Abstract

The ability to detect errors and adjust behavior accordingly is essential for maneuvering in an uncertain environment. Errors are particularly prone to occur when multiple, conflicting responses are registered in a situation that requires flexible behavioral outputs. Previous studies have provided evidence indicating the importance of the medial cortical brain regions including the cingulate cortex in processing conflicting information. However, conflicting situations can be successfully resolved, or lead to errors, prompting a behavioral change in the observers. In particular, how does the brain use error signals specifically to adjust behavior on the fly? Here we employ a stop signal task (SST) to elicit errors approximately half of the time in high-conflict trials despite constant behavioral adjustment of the observers. Using functional magnetic resonance imaging, we show greater and, sequentially, less activation in the medial cortical regions when observers made an error, compared to when they successfully resolved high-conflict responses. Errors also evoked greater activity in the cuneus, retrosplenial cortex, insula, and subcortical structures including the thalamus and the region of the epithalamus (the habenula). We further showed that the error-related medial cortical activities are not correlated with post-error behavioral adjustment, as indexed by post-error slowing (PES) in go trial reaction time. These results delineate an error-specific pattern of brain activation during the SST. The results also suggest that the relationship between error-related activity and post-error behavioral adjustment may be more complicated than has been conceptualized by the conflict monitoring hypothesis.

Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI

“…Errors are typically considered as rare, negative and interfering events, which need to be avoided, and can even activate the defensive/aversive motivational system (Hajcak & Foti, 2008). Accordingly, it is plausible that errors do not only influence cognitive mechanisms such as learning, attention, and memory, but also modulate affective states in order to promote adaptive and flexible behaviors (Hajcak et al, 2005;Li et al, 2008). Nevertheless, very few studies have corroborated this assumption so far (see Brazdil et al, 2002), and the impact of errors on brain systems implicated in emotional appraisal remains largely unknown.…”

“…Nevertheless, very few studies have corroborated this assumption so far (see Brazdil et al, 2002), and the impact of errors on brain systems implicated in emotional appraisal remains largely unknown. Some preliminary evidence comes from functional neuroimaging studies that reported activations to errors in regions usually associated with emotional processing such as the amygdala or insula (Menon et al, 2001;Garavan et al, 2002;Polli et al, 2008Polli et al, , 2009Li et al, 2008). However, these studies do not inform about the exact time-course of error processing, in particular in relation to successive stages of motor preparation, execution, and/or feedback signals.…”

“…Based on this evidence, some theories proposed that ACC activity following errors could also reflect an appraisal of the affective significance or salience of errors (Luu, Tucker, Derryberry, Reed, & Poulsen, 2003;Hajcak, Moser, Yeung, & Simons, 2005;Pizzagalli, Peccoralo, Davidson, & Cohen, 2006;Taylor et al, 2006;Polli et al, 2008Polli et al, , 2009Li et al, 2008;Hajcak & Foti, 2008). Consistent with this notion, the amplitude of the ERN is modulated not only by manipulations such as the frequency of errors (as predicted by the error-based reinforcement learning model, see Gehring, Goss, Coles, Meyer, & Donchin, 1993;Hajcak et al, 2003b), but also by motivational and emotional factors unrelated to the dopaminergic reward system, such as changes in state or trait anxiety (see Hajcak, McDonald, & Simons, 2003aVocat, Pourtois, & Vuilleumier, 2008; see also Pizzagalli et al, 2006).…”

“…Because both the amygdala and insula are implicated in anxiety and defensive behaviors, these limbic regions might also contribute to error detection processes taking place in dorsal ACC (Ochsner & Gross, 2005;Fales et al, 2008;Kienast et al, 2008). Indirect evidence in support of this theory comes from a few neuroimaging studies that showed increased activity to errors not only in ACC and PFC, but also in deeper limbic brain structures such as the amygdala, insula, and thalamus (Menon, Adleman, White, Glover, & Reiss, 2001;Garavan, Ross, Murphy, Roche, & Stein, 2002;Polli et al, 2008;Li et al, 2008). In a recent fMRI study, Polli et al (2009) reported an interesting association between the amygdala and rostral ACC during action monitoring, although reliable differences between the left and right amygdala were found in this study.…”

Biological markers of the effects of intravenous methylphenidate on improving inhibitory control in cocaine-dependent patients

“…We used a simple reaction time task in this stop signal paradigm (39,40,(63)(64)(65). There were two trial types, "go" and "stop," randomly intermixed.…”