George A. Buzzell

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

&NA; 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. HighlightsERN topography and source activity changed as a function of age (9–35 years).Two primary clusters of neural activity found to give rise to the ERN.Dorsal cluster stable across age, ventral‐frontal cluster increased with age.Dorsal cluster (including posterior cingulate) predicted control after errors.Data serve as model of typical error‐monitoring development.

Mu rhythm desynchronization is specific to action execution and observation: Evidence from time-frequency and connectivity analysis

&NA; Mu desynchronization is the attenuation of EEG power in the alpha frequency range recorded over central scalp locations thought to reflect motor cortex activation. Mu desynchronization during observation of an action is believed to reflect mirroring system activation in humans. However, this notion has recently been questioned because, among other reasons, the potential contamination of mu rhythm and occipital alpha activity induced by attention processes following presentation of visual stimuli in observation conditions. This study examined the validity of mu desynchronization as a measure of mirroring system activation in infants and further investigated the pattern of functional connectivity between the central and occipital regions during execution and observation of movement. EEG was recorded while 46 9‐month‐old infants executed grasping actions and observed an experimenter grasping. Current source density (CSD) was applied to EEG data and, time‐frequency and connectivity analyses were performed in CSD transformed data. Mu desynchronization was evident over central regions during both execution and observation of movements. Independent alpha desynchronization over occipital region was also present in both conditions. The connectivity analyses revealed that central‐occipital areas were functionally more connected compared to other areas of the brain during observation of movements. Collectively, the results demonstrate the validity of mu desynchronization as an index of infant mirroring system activity and support the proposal of a functional connection between distinct mirroring and attention processes during observation of action. HighlightsObservation of a movement evoked mirroring activity in infants.Mirroring activity began before observed movement suggesting anticipation the movement.Motor and occipital areas were functionally coupled during movement observation.Mu desynchronization can be used as a valid index of mirroring activity in infant.

Adolescent Cognitive Control, Theta Oscillations, and Social Motivation

Cognitive control supports goal-directed behavior and involves two main components: 1) monitoring for situations requiring control, such as errors or conflict; 2) control recruitment, either proactively before needed or reactively in a just-in-time manner. In adults, increased theta power over medial-frontal cortex (MFC) underlies monitoring, whereas theta connectivity between MFC and lateral-frontal regions reflects control recruitment. Theta oscillations have been proposed as an organizing principle of cognitive control in human adults and are conserved across species. However, theta’s role in supporting adolescent cognitive control remains unclear. Moreover, adolescence is characterized by a motivation-control mismatch, with social motivation being particularly salient. Characterizing theta band dynamics could clarify motivational influences on cognitive control during this developmental window. Here, we investigated theta dynamics while adolescents performed a flanker task twice, once alone and once believing they were under peer observation to increase social motivation. Broadly, theta dynamics were found to behave qualitatively similar to prior reports in adults. In a novel approach, we separated theta dynamics immediately before and after motor responses, identifying specific cognitive control mechanisms. We dissociate MFC connectivity with rostral/caudal frontal cortex and distinct forms of post-error behavioral control, as well as identified inverse relations between pre- and post-response control. Finally, social motivation was found to exclusively upregulate post-response error monitoring and proactive control, as opposed to pre-response conflict monitoring and reactive control. Collectively, the current study links theta to adolescent cognitive control, identifies specific effects of social motivation on proactive control, and more broadly identifies novel cognitive control dynamics. Significance Statement Cognitive control reflects neurocognitive processes that allow for goal-directed behavior. Prior work links theta band neural oscillations (4-8 Hz) to cognitive control in adults, however research during adolescence is limited and relations to social motivation unclear. Here, we identify clear links between theta and cognitive control within adolescents. Moreover, leveraging analysis of neural oscillations we parse cognitive control into subprocesses, finding social motivation to selectively upregulate self-detection of errors and changes in control to prevent future errors. Linking adolescent cognitive control to theta oscillations provides a bridge between non-invasive recordings in humans and mechanistic studies of neural oscillations in animal models; links to social motivation provide insight into the nuanced motivation-control interactions that occur during adolescence.

Time-frequency approaches to investigating changes in feedback processing during childhood and adolescence

Processing feedback from the environment is an essential function during development to adapt behavior in advantageous ways. One measure of feedback processing, the feedback negativity (FN), is an ERP observed following the presentation of feedback. Findings detailing developmental changes in the FN have been mixed, possibly due to limitations in traditional ERP measurement methods. Recent work shows that both theta and delta frequency activity contribute to the FN; utilizing time-frequency methods to measure change in power and phase in these frequency bands may provide more accurate representation of feedback processing development in childhood and adolescence. We employ time-frequency power and intertrial phase synchrony measures, in addition to conventional time-domain ERP methods, to examine the development of feedback processing in the theta (4-7 Hz) and delta (.1-3 Hz) bands throughout adolescence. A sample of 54 female participants (8-17 years old) completed a gambling task while EEG was recorded. As expected, time-domain ERP amplitudes showed no association with age. In contrast, significant effects were observed for the time-frequency measures, with theta power decreasing with age and delta power increasing with age. For intertrial phase synchrony, delta synchrony increased with age, while age-related changes in theta synchrony differed for gains and losses. Collectively, these findings highlight the importance of considering time-frequency dynamics when exploring how the processing of feedback develops through late childhood and adolescence. In particular, the role of delta band activity and theta synchrony appear central to understanding age-related changes in the neural response to feedback.

Relations between Behavioral Inhibition, Cognitive Control, and Anxiety: Novel Insights Provided by Parsing Subdomains of Cognitive Control

The temperament of behavioral inhibition (BI) is classically defined based on behavioral observations of a child’s fear and avoidance of novelty. Such behavioral observations have proven powerful in identifying individual differences in temperament, and such differences have been shown to be predictive of later developmental outcomes, particularly levels of shyness or anxiety. However, behavioral observations alone leave open several questions, including: (1) How does the brain of a child high in behavioral inhibition differ from a child low in behavioral inhibition? (2) Which domains of cognition are directly related to variation in behavioral inhibition? (3) For domains of cognition not directly related to behavioral inhibition, how do individual differences interact with behavioral inhibition to predict later risk for anxiety? Examining these questions, research has demonstrated that individual differences in the child’s ability to monitor and control their behaviors when trying to complete a goal, a set of processes known as “cognitive control,” may change the likelihood of a child high in behavioral inhibition developing later anxiety. However, relations between behavioral inhibition and cognitive control have been inconsistent across studies. Here, we leverage a cognitive neuroscience framework to review studies that have investigated the interrelations between behavioral inhibition, cognitive control, and anxiety. Critically, we separate cognitive control into the subdomains of “monitoring” and “control instantiation” as well as further parse control instantiation based on domain and time course. In making these distinctions, we show that there is consistent evidence that the behavioral inhibition phenotype is directly related to increased monitoring, but not levels of control instantiation. However, behavioral inhibition is related to the time course of control, and both monitoring and control interact with behavioral inhibition to predict increased risk for the development of anxiety. We suggest that continued progress in understanding the interrelations between behavioral inhibition and cognitive control will require a similar framework that separates cognitive control into subdomains.

Speeded response errors and the error-related negativity modulate early sensory processing

&NA; Empirical research demonstrates that when the time following error commission is constrained, subsequent sensory processing can be impaired (Buzzell et al., 2017). This reduction in sensory processing is presumably due to a bottleneck for cognitive resources produced by an overlap between error processing and subsequent stimulus processing. This finding suggests that the system dedicated to improving task performance can actually sometimes be the source of performance failures. Although this finding established that data‐limited errors lead to a reduction in sensory processing at short response stimulus intervals (RSIs), it remains unclear if the relationship between error processing and subsequent sensory processing can be modulated by speeded‐response errors. In the present study, event‐related potentials and behavioral measures were recorded while participants performed a modified version of a Simon task, in which RSI duration was varied. We found that sensory processing, indexed by the P1 component, was reduced following errors at short (200–533 ms), but not long (866–1200 ms), RSIs. Moreover, the magnitude of error processing differentially influenced subsequent sensory processing as a function of RSI. However, whereas prior work demonstrated that the error positivity (Pe) modulated sensory processing on the subsequent trial, only the error‐related negativity (ERN) did so within the Simon task. This suggests that although both data‐limited errors and speeded‐response errors can impact subsequent sensory processing, different stages of error processing appear to mediate this phenomenon.

Reward Processing in Depression: A Conceptual and Meta-Analytic Review Across fMRI and EEG Studies

OBJECTIVE: A role for aberrant reward processing in the pathogenesis of depression has long been proposed. However, no review has yet examined its role in depression by integrating conceptual and quantitative findings across functional MRI (fMRI) and EEG methodologies. The authors quantified these effects, with an emphasis on development. METHOD: A total of 38 fMRI and 12 EEG studies were entered into fMRI and EEG meta-analyses. fMRI studies primarily examined reward anticipation and reward feedback. These were analyzed using the activation likelihood estimation method. EEG studies involved mainly the feedback-related negativity (FRN) event-related potential, and these studies were analyzed using random-effects meta-analysis of the association between FRN and depression. RESULTS: Analysis of fMRI studies revealed significantly reduced striatal activation in depressed compared with healthy individuals during reward feedback. When region-of-interest analyses were included, reduced activation was also observed in reward anticipation, an effect that was stronger in individuals under age 18. FRN was also significantly reduced in depression, with pronounced effects in individuals under age 18. In longitudinal studies, reduced striatal activation in fMRI and blunted FRN in EEG were found to precede the onset of depression in adolescents. CONCLUSIONS: Taken together, the findings show consistent neural aberrations during reward processing in depression, namely, reduced striatal signal during feedback and blunted FRN. These aberrations may underlie the pathogenesis of depression and have important implications for development of new treatments.