Development of the error-monitoring system from ages 9–35: Unique insight provided by MRI-constrained source localization of EEG

Abstract

The ability to self-detect errors and dynamically adapt behavior is a cornerstone of higher-level cognition, requiring coordinated activity from a network of neural regions. However, disagreement exists over how the error-monitoring system develops throughout adolescence and early adulthood. The present report leveraged MRI-constrained EEG source localization to detail typical development of the error-monitoring system in a sample of 9–35 year-olds (n=43). Participants performed a flanker task while high-density EEG was recorded; structural MRIs were also acquired for all participants. Analysis of the scalp-recorded EEG data revealed a frontocentral negativity (error-related negativity; ERN) immediately following errors for all participants, although the topography of the ERN varied with age. Source localization of the ERN time range revealed maximal activity within the posterior cingulate cortex (PCC) for all ages, consistent with recent evidence that the PCC provides a substantial contribution to the scalp-recorded ERN. Activity within a network of brain regions, including dorsal anterior cingulate, PCC, and parietal cortex, was predictive of improved performance following errors, regardless of age. However, additional activity within insula, orbitofrontal cortex and inferior frontal gyrus linearly increased with age. Together, these data suggest that the core error-monitoring system is online by early adolescence and remains relatively stable into adulthood. However, additional brain regions become embedded within this core network with age. These results serve as a model of typical development of the error-monitoring system from early adolescence into adulthood.

A Neurobehavioral Mechanism Linking Behaviorally Inhibited Temperament and Later Adolescent Social Anxiety

“…Specifically, we demonstrate that early-life BI temperament predicts later hypersensitivity toward errors while under social scrutiny, particularly for females (see Figure S6, available online). Moreover, we found no direct relation between hypersensitivity toward errors and social anxiety in adolescence, which could reflect immaturity in the performance-monitoring system 11 as a direct relation has been found in adults. 16 Finally, direct relations with adolescent social anxiety were found for error preoccupation, and the patterns in other portions of the data extended prior models of social anxiety and BI, 17,18 with BI predicting error hypersensitivity, and in turn, error preoccupation correlating with concurrent social anxiety symptoms.…”

“…7,8 This measure of performance monitoring 9 is sensitive to error salience, 10 consistent with the notion that BI children display hypersensitivity toward errors. Risk for anxiety among children with BI is increased for those with a relatively large (more negative) ERN, 7,8 possibly reflecting functioning in a salience network 11 encompassing the cingulate, 12 insula, and orbitofrontal cortex 13 —regions also associated with risk for anxiety. 14 However, although the ERN elicited by standard laboratory tasks is useful for identifying BI children at heightened risk for anxiety, this moderation provides incomplete information on mechanisms underlying the link between BI and social anxiety.…”

“…16 However, because both ERN and social anxiety change in the peri-adolescent period, 11 relations between ERN and anxiety may also change. Cognitive models suggest a framework for testing ideas relating neural, behavioral, and social effects in the peri-adolescent period, when peers become increasingly salient.…”

Impact of pubertal timing and depression on error‐related brain activity in anxious youth

“…In line with this possibility, prior work suggests there is a degree of normative developmental increase in the ERN (Buzzell et al, 2017). Theoretically, increased ERN in adolescence is thought to reflect the transition from sensitivity to external fear to greater internal saliency of threats related to ones’ behavior (Meyer, 2017).…”

“…The ERN was initially localized primarily to the anterior cingulate cortex (van Veen & Carter, 2002), a region of the brain where information about pain, threat, and punishment is integrated to change behavior (Shackman et al, 2011). Additionally, more recent work suggests that activity within the posterior cingulate cortex (Buzzell et al, 2017), superior/medial prefrontal cortex (Hochman, Eviatar, Breznitz, Nevat, & Shaul, 2009; Holmes & Pizzagalli, 2008), and insular cortex (Czobor et al, 2017), which operate within a fronto-limbic network involved in emotional salience and attention, also provide a substantial contribution to the scalp-recorded ERN. An enhanced ERN is postulated to be involved in conflict monitoring (Yeung, Botvinick, & Cohen, 2004), increased sensitivity to endogenous threat (Weinberg, Meyer, et al, 2016), and reinforcement learning (Holroyd & Coles, 2002).…”