Variability in post‐error behavioral adjustment is associated with functional abnormalities in the temporal cortex in children with ADHD

Error processing is an executive control process that refers to the detection of an error and the subsequent behavioral adjustment (Gehring & Fencsik, 2001; Taylor, Stern & Gehring, 2007). When healthy adults and children are engaged in a fast reaction time tasks, error processing is reflected by longer reaction times (RT) on trials immediately following the error (post-error trials) (Rabbitt, 1966; Sergeant & van der Meere, 1988). This post-error slowing is interpreted as a sign of ongoing cognitive control processes, allowing subsequent improvement in task performance. Functional magnetic resonance imaging (fMRI) and electrophysiological findings have identified the posterior part of the medial frontal cortex (pMFC), which comprises the dorsal anterior cingulate cortex (dACC), and the lateral prefrontal cortex (PFC), as key regions involved in error processing and subsequent behavioral adjustment. Although the specific role of these regions is unclear, it has been suggested that the pMFC may be important during error monitoring while the lateral PFC may be recruited to regulate subsequent task performance (Ridderinkhof et al., 2004; Taylor et al., 2007). In healthy adults, fMRI studies using fast response inhibition tasks, including the Go/No-Go and the Stop-Signal tasks, have consistently reported activation of the dACC when comparing error versus correct inhibition trials (Hester, Fassbender & Garavan, 2004; Menon et al., 2001), and increased ventrolateral PFC when comparing post-error versus post-correct inhibition trials (Li et al., 2008). Error processing abnormalities in children with Attention-Deficit Hyperactivity Disorder (ADHD) have been previously reported in electrophysiological and behavioral studies. Specifically, children with ADHD fail to exhibit the post-error slowing that is seen in typically developing (TD) children and show high intra-subject variability (ISV) in their post-error RT (Epstein et al., 2009; Schachar et al., 2004; Sergeant & van der Meere, 1988; Wiersema, van der Meere & Roeyers, 2005). Moreover, a decrease in electrophysiological components associated with error processing, the error-related negativity (ERN) and error positivity (Pe), has been reported in children with in ADHD using a variety of paradigms (Liotti et al., 2005; Overtoom et al., 2002; Wiersema et al., 2005, see also review by Shiels & Hawk 2010). Moreover, recent electrophysiological data in adolescents with ADHD using the Go/No-go task show a significant reductions in late evoked theta power and early and late theta inter-trial phase coherence, suggesting suggest that a weaker error-related signal from the ACC to the PFC, important for guiding future behavior, may underline poor performance in ADHD (Groom et al. 2010). Data on the neural correlates of error processing in children with ADHD are limited and findings from existing studies are inconsistent. Pliszka et al. (2006) contrasted unsuccessful and successful Stop-Signal trials, and found that children with ADHD fail to show patterns of dACC and ventrolateral PFC activation observed in TD children (Pliszka et al., 2006). These findings align with previous studies reporting decreased ERN in ADHD, the electrophysiological component considered to be localized in the dACC (Liotti et al., 2005), and suggest that reduced dACC activity in ADHD may compromise recruitment of ventrolateral PFC regions involved in post-error behavioral adjustment. In contrast, Rubia et al. (2005) found that adolescents with ADHD exhibited reduced activation in the precuneus and posterior cingulate cortex (PCC), relative to controls, when unsuccessful inhibition trials were compared to go trials (Rubia et al., 2005). The PCC is important for the allocation of visuospatial attention (Mohanty et al., 2008). Attentional fluctuations are hypothesized to compete with goal-directed activity and affect task performance by increasing intra-subject variability (ISV) in responding (Sonuga-Barke & Castellanos, 2007). Increased ISV in response RT is a consistent finding in ADHD (Castellanos & Tannock, 2002; Vaurio, Simmonds & Mostofsky, 2009). Therefore it is possible that error processing deficits in ADHD are related to attentional impairments and abnormal precuneus/PCC neural activity. While these studies have provided some initial insight into the neural correlates of error processing in children with ADHD, no studies have examined whether the behavioral findings of decreased RT slowing and increased ISV for post-error trials are related to functional abnormalities of the dACC, the precuneus/PCC, or both. The present study examines the neural correlates of error processing in children with ADHD using fMRI and the Go/No-Go task by comparing neural activity during two contrasts, errors versus correct inhibition trials and post-error versus post-correct inhibition trials. Based on previous data, we hypothesized that children with ADHD would show less RT slowing and higher ISV on post-error trials compared to TD children. We further predicted that, compared to TD children, children with ADHD would show decreased activation in both the dACC and the precuneus/PCC in during error trials, and would show reduced ventrolateral PFC activation during post-error trials.