Prefrontal modulation of frustration-related physiology in preschool children ranging from low to severe irritability

Grabell, Adam S.; Santana, Adrelys Mateo; Thomsen, Kari N.; Gonzalez, Katie; Zhang, Zhongyang; Bivins, Zachary; Rahman, Tauhidur

doi:10.1016/j.dcn.2022.101112

Cited by 4 publications

(2 citation statements)

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“…Increased irritability has been linked to poor cognitive flexibility task performance [ 30 ] and incapacity to adjust to altering environmental demands [ 31 ]. Along with behavior, the relationship between irritability and cognitive flexibility has been identified at the neural level [ 32 , 33 , 34 , 35 ]. For example, using episodic irritability-eliciting tasks (i.e., tasks that induce frustration), increased prefrontal activation has been found in adults [ 36 ] and children [ 34 , 37 , 38 ], which has been related to elevated irritability [ 34 , 39 , 40 ].…”

Section: Introductionmentioning

confidence: 99%

Irritability Moderates the Association between Cognitive Flexibility Task Performance and Related Prefrontal Cortex Activation in Young Children

Grabell

Perlman

2023

Brain Sciences

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The association between cognitive flexibility and related neural functioning has been inconsistent. This is particularly true in young children, where previous studies have found heterogenous results linking behavior and neural function, raising the possibility of unexplored moderators. The current study explored the moderating role of dimensional irritability in the association between cognitive flexibility task performance and prefrontal activation in young children. A total of 106 3- to 7-year-old children were recruited to complete a custom-designed, child-adapted, cognitive flexibility task, and 98 of them were included in the data analysis. The children’s dorsolateral prefrontal cortex activation was monitored using functional near-infrared spectroscopy, and their levels of irritability were reported by parents using the MAP-DB Temper Loss subscale. Results indicated that the mean reaction time of the cognitive flexibility task was negatively correlated with concurrent prefrontal activation. No evidence was found for the association between task accuracy and prefrontal activation. Moreover, irritability moderated the association between the mean reaction time and prefrontal activation. Children high in irritability exhibited a stronger negative association between the mean reaction time and related prefrontal activation than children low in irritability. The moderating model suggested a novel affective–cognitive interaction to investigate the associations between cognitive task performance and their neural underpinnings.

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Section: Introductionmentioning

confidence: 99%

Irritability Moderates the Association between Cognitive Flexibility Task Performance and Related Prefrontal Cortex Activation in Young Children

Grabell

Perlman

2023

Brain Sciences

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“…In an interpersonal context, for children who experience a lowered threshold for frustration, the intensity of this emotional state can engender socially disruptive responses (e.g., tantrums/emotional outbursts) (Carlson et al., 2022; Leibenluft, 2017a). Behavioral and neural research, which generally employ paradigms to deliberately obstruct a desired goal (Grabell et al., 2022; Perlman et al., 2015; Quiñones‐Camacho et al., 2020), has established that irritable youth are especially likely to experience frustrative response due to abnormal processing of reward‐related information (Brotman, Kircanski, & Leibenluft, 2017; Brotman, Kircanski, Stringaris, et al., 2017). A neural circuit including the ventromedial and orbitofrontal cortices (vmPFC/OFC), inferior frontal gyrus (IFG), anterior cingulate (ACC), and caudate has been implicated in facilitating reward processing (Kahnt, 2018; Wang et al., 2016).…”

Section: Introductionmentioning

confidence: 99%

A network approach to the investigation of childhood irritability: probing frustration using social stimuli

Thompson,

Schneider,

Lopez‐Roque

et al. 2023

Child Psychology Psychiatry

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BackgroundSelf‐regulation in early childhood develops within a social context. Variations in such development can be attributed to inter‐individual behavioral differences, which can be captured both as facets of temperament and across a normal:abnormal dimensional spectrum. With increasing emphasis on irritability as a robust early‐life transdiagnostic indicator of broad psychopathological risk, linkage to neural mechanisms is imperative. Currently, there is inconsistency in the identification of neural circuits that underlie irritability in children, especially in social contexts. This study aimed to address this gap by utilizing a functional magnetic resonance imaging (fMRI) paradigm to investigate pediatric anger/frustration using social stimuli.MethodsSeventy‐three children (M = 6 years, SD = 0.565) were recruited from a larger longitudinal study on irritability development. Caregivers completed questionnaires assessing irritable temperament and clinical symptoms of irritability. Children participated in a frustration task during fMRI scanning that was designed to induce frustration through loss of a desired prize to an animated character. Data were analyzed using both general linear modeling (GLM) and independent components analysis (ICA) and examined from the temperament and clinical perspectives.ResultsICA results uncovered an overarching network structure above and beyond what was revealed by traditional GLM analyses. Results showed that greater temperamental irritability was associated with significantly diminished spatial extent of activation and low‐frequency power in a network comprised of the posterior superior temporal sulcus (pSTS) and the precuneus (p < .05, FDR‐corrected). However, greater severity along the spectrum of clinical expression of irritability was associated with significantly increased extent and intensity of spatial activation as well as low‐ and high‐frequency neural signal power in the right caudate (p < .05, FDR‐corrected).ConclusionsOur findings point to specific neural circuitry underlying pediatric irritability in the context of frustration using social stimuli. Results suggest that a deliberate focus on the construction of network‐based neurodevelopmental profiles and social interaction along the normal:abnormal irritability spectrum is warranted to further identify comprehensive transdiagnostic substrates of the irritability.

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Understanding irritability through the lens of self-regulatory control processes in children and adolescents: a systematic review

Urben,

Ochoa Williams,

Ben Jemia

et al. 2024

Eur Child Adolesc Psychiatry

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Among youths, pathological irritability is highly prevalent and severely disabling. As a frequent symptom, it often leads to referrals to child and adolescent mental health services. Self-regulatory control (SRC) processes are a set of socio-psycho-physiological processes that allow individuals to adapt to their ever-changing environments. This conceptual framework may enhance the current understanding of the cognitive, emotional, behavioural and social dysregulations underlying irritability. The present systematic review (PROSPERO registration: #CRD42022370390) aims to synthesize existing studies that examine irritability through the lens of SRC processes among youths (< 18 years of age). We conducted a comprehensive literature search among six bibliographic databases: Embase.com, Medline ALL Ovid, APA PsycInfo Ovid, Web of Science Core Collection, the Cochrane Database of Systematic Reviews Wiley and ProQuest Dissertations & Theses A&I. Additional searches were performed using citation tracing strategies. The retrieved reports totalled 2612, of which we included 82 (i.e., articles) from 74 studies. More than 85% of reports were published during the last 6 years, highlighting the topicality of this work. The studies sampled n = 26,764 participants (n = 12,384 girls and n = 12,905 boys, n = 1475 no information) with an average age of 8.08 years (SD = 5.26). The included reports suggest that irritability has an association with lower effortful control, lower cognitive control and delay intolerance. Further, evidence indicates both cross-sectional and longitudinal associations between irritability and a lack of regulation skills for positive and negative emotions, particularly anger. Physiological regulation seems to moderate the association between irritability and psychopathology. Finally, the mutual influence between a child’s irritability and parenting practice has been established in several studies. This review uses the lens of SRC to illustrate the current understanding of irritability in psychopathology, discusses important gaps in the literature, and highlights new avenues for further research.

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Prefrontal modulation of frustration-related physiology in preschool children ranging from low to severe irritability

Cited by 4 publications

References 67 publications

Irritability Moderates the Association between Cognitive Flexibility Task Performance and Related Prefrontal Cortex Activation in Young Children

Irritability Moderates the Association between Cognitive Flexibility Task Performance and Related Prefrontal Cortex Activation in Young Children

A network approach to the investigation of childhood irritability: probing frustration using social stimuli

Understanding irritability through the lens of self-regulatory control processes in children and adolescents: a systematic review

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