Error-signaling in the developing brain

Abstract

While learning from mistakes is a lifelong process, the rate at which an individual makes errors on any given task decreases through late adolescence. Previous fMRI adult work indicates that several control brain networks are reliably active when participants make errors across multiple tasks. Less is known about the consistency and localization of error processing in the child brain because previous research has used single tasks. The current analysis pooled data across three studies to examine error-related task activation (two tasks per study, three tasks in total) for a group of 232 children aged 8–17 years. We found that, consistent with the adult literature, the majority of applied cingulo-opercular brain regions, including medial superior frontal cortex, dorsal anterior cingulate, and bilateral anterior insula, showed consistent error processing engagement in children across multiple tasks. Error-related activity in many of these cingulo-opercular regions correlated with task performance. However, unlike in the adult literature, we found a lack of error-related activation across tasks in dorsolateral frontal areas, and we also did not find any task-consistent relations with age in these regions. Our findings suggest that the task-general error processing signal in the developing brain is fairly robust and similar to adults, with the exception of lateral frontal cortex.

Multimodal study of the neural sources of error monitoring in adolescents and adults

“…Neuroimaging studies using fMRI find strong activation in frontal brain areas on tasks requiring relatively high levels of conflict resolution. These areas include the dACC and other cingulo‐opercular regions, dorsolateral prefrontal cortex (DLPFC), and other prefrontal regions (Carter et al, 1998; MacDonald et al, 2000; Ridderinkhof et al, 2004; Roe et al, 2021; Taylor et al, 2007; van Veen et al, 2001). The dACC is more active in various tasks requiring performance monitoring and error detection (Le et al, 2021; Nee et al, 2007; Ridderinkhof et al, 2004; Weiss & Luciana, 2022).…”

“…Age differences in error monitoring skill manifest in the ERN ERP (Buzzell, Richards, et al, 2017; Davies et al, 2004; Gavin et al, 2019; Ladouceur et al, 2007; Lo, 2018; Overbye et al, 2019; Roe et al, 2021; Taylor et al, 2018; for reviews, see Boen et al, 2022; Lo, 2018; Tamnes et al, 2013). Lo (Lo, 2018) reported a meta‐analysis of the developmental changes in the ERN and N21 from childhood to adulthood.…”

Software Bug Detection Causes a Shift From Bottom-Up to Top-Down Effective Connectivity Involving the Insula Within the Error-Monitoring Network

“…In contrast, for the code with bugs, when the participants search for bugs, a set of anterior/frontal decision-related regions show a causal relation with insular activity. These areas include Brodmann area (BA) 6 and 8, which are the medial prefrontal cortex regions involved in memory, reasoning, error detection, or attention ( Iannaccone et al, 2015 ), and most importantly, the regions of the anterior cingulate cortex (ACC) (BA 24 and 32), which are the well-known regions of the error-monitoring circuitry ( Gilbertson et al, 2020 ; Roe et al, 2021 ). This suggests a posterior-to-anterior shift of causal influences to the insula when error detection is required.…”

“…Evidence that the insular cortex also seems to be involved in performance monitoring ( Bastin et al, 2017 ; Billeke et al, 2020 ) and our Granger causality findings showing that error-monitoring-related activity triggers a shift of causal influences to frontal regions, in particular, ACC, make a strong basis toward the notion that the insula is a pivotal region during error-monitoring. Future studies should elucidate how this anterior reconfiguration of connectivity generalizes to other tasks, in children and adults’ learning ( Roe et al, 2021 ).…”

Key considerations for child and adolescent MRI data collection

“…For example, some skills continue to improve (e.g., executive function) throughout development, some skills show early growth and then plateau (e.g., response speed tasks), while some skills aren't present consistently in a given age sample (i.e., word reading in 5-7 year-olds). One type of task design that can adjust performance dynamically over time to keep participants at a similar level of performance is "staircasing"; this approach has been used most often in inhibition tasks (e.g., Roe et al, 2021). While staircasing is not appropriate for many tasks, considering the influence of task performance on research objectives, and doing careful behavioral piloting prior to MRI scanning is clearly essential for high-quality task fMRI data.…”