Implications of ongoing neural development for the measurement of the error‐related negativity in childhood

Abstract

Event-related potentials (ERPs) have been proposed as biomarkers capable of reflecting individual differences in neural processing not necessarily detectable at the behavioral level. However, the role of ERPs in developmental research could be hampered by current methodological approaches to quantification. ERPs are extracted as an average waveform over many trials, however, actual amplitudes would be misrepresented by an average if there was high trial-to-trial variability in signal latency. Low signal temporal consistency is thought to be a characteristic of immature neural systems, although consistency is not routinely measured in ERP research. The present study examined the differential contributions of signal strength and temporal consistency across trials in the error-related negativity (ERN) in 6-year-old children, as well as the developmental changes that occur in these measures. The 234 children were assessed annually in kindergarten, 1st, and 2nd grade. At all assessments signal strength and temporal consistency were highly correlated with the average ERN amplitude, and were not correlated with each other. Consistent with previous findings, ERN deflections in the averaged waveform increased with age. This was found to be a function of developmental increases in signal temporal consistency, whereas signal strength showed a significant decline across this time period. Additionally, average ERN amplitudes showed low-to-moderate stability across the three assessments whereas signal strength was highly stable. In contrast, signal temporal consistency did not evidence rank order stability across these ages. Signal strength appears to reflect a stable individual trait whereas developmental changes in temporal consistency may be experientially influenced.

Early math and reading achievement are associated with the error positivity

“…The error-related negativity (ERN) is an ERP component that is elicited when an individual makes a mistake on a speeded target discrimination task, and is thought to reflect error detection and conflict resolution processes associated with monitoring one’s responses (Falkenstein, Hohnsbein, Hoormann, & Blanke, 1991; Gehring, Goss, Coles, Meyer, & Donchin, 1993; see Gehring, Liu, Orr, & Carp, 2012, for a review). Evidence suggests that the ERN is sensitive to development, such that older individuals exhibit a larger ERN (e.g., Davies, Segalowitz, & Gavin, 2004; DuPuis et al, 2015). A larger ERN is positively associated with undergraduate student grades; stronger grades may be linked to a greater ability to monitor one’s performance and engage cognitive control mechanisms (Hirsh & Inzlicht, 2010).…”

ERN, theta power, and risk for anxiety problems in preschoolers

“…The ERN has been the subject of numerous empirical studies aimed at delineating its precise function and association(s) with behavior (e.g., Brooker, Buss, & Dennis, 2011; Brooker & Buss, 2014; DuPuis et al, 2015; Holroyd & Coles, 2002; Jonkman et al, 2007; Ladouceur et al, 2007; Meyer et al, 2012; Torpey, Hajcak, & Klein, 2009; Torpey et al, 2012). Although significant advances have been made, much remains to be understood about the ERN as part of a coordinated network of neural responses during development.…”

“…This difference is presumably due to a maturational shift from a reliance on parietal brain regions for processes of self-monitoring to increasing dependence on the maturing frontal cortex (Durston et al, 2006). ERN amplitudes also appear to change over time, typically increasing with age (Du Puis et al, 2015, though see also Grammer, Carrasco, Gehring, & Morrison, 2014). The ERN in children peaks between −4 (Ladouceur, Dahl, & Carter, 2007) and −7.35 microvolts (Du Puis et al, 2015) while adult ERN peaks between −5 and −10 microvolts (Hajcak et al, 2005; Moser, Hajcak, & Simons, 2005).…”

“…ERN amplitudes also appear to change over time, typically increasing with age (Du Puis et al, 2015, though see also Grammer, Carrasco, Gehring, & Morrison, 2014). The ERN in children peaks between −4 (Ladouceur, Dahl, & Carter, 2007) and −7.35 microvolts (Du Puis et al, 2015) while adult ERN peaks between −5 and −10 microvolts (Hajcak et al, 2005; Moser, Hajcak, & Simons, 2005). Developmental changes in ERN amplitudes are believed to reflect the maturation of neural structures, such as the anterior cingulate cortex (ACC), from which the ERN is believed to originate (Carter et al, 1998).…”

“…Greater ERN amplitudes are associated with more anxious behaviors in children ages 8-14 (Ladouceur, Dahl, & Carter, 2007) and greater negative affect (Hajcak & Foti, 2008) and increased sensitivity to the value of errors (Hajcak, Moser, Yeung, & Simons, 2005) in young adults. Greater ERN is also linked with poorer attentional orienting in 4-8 year-old children (Brooker, Buss, & Dennis, 2011), but better executive functioning and more positive academic outcomes in children between ages 5 and 8 (DuPuis, Ram, Willner, Karalunas, Segalowitz, & Gatzke-Kopp, 2015). …”