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Influences of affective context on amygdala functional connectivity during cognitive control from adolescence through adulthood.

ABSTRACT: Emotion processing is believed to dominate over other brain functions during adolescence, including inhibitory control. However, few studies have examined the neural underpinnings of affective states during cognitive control. Here, we characterized the brain in an affective state by cross-sectionally assessing age-related changes in amygdala background connectivity during an affective inhibitory control task. Participants completed an antisaccade (AS) fMRI task while affective auditory stimuli were presented, and a 5-minute resting state scan. Results showed that while adolescents reported similar arousal levels across emotional conditions, adults perceived negative sounds to be more "arousing" and performed better than adolescents in negative trials. Amygdala background connectivity showed age-related increases with brain regions related to attention and executive control, which were not evident during resting state. Together, results suggest that amygdala connectivity within an affective context is fairly low in mid-adolescence but much stronger in adulthood, supporting age-related improvements in inhibitory control within an affective state. These findings suggest limitations during adolescence in differentiating between the arousing effects of various emotions, potentially undermining the ability to optimally engage inhibitory control. Furthermore, the age-related fMRI findings suggest that low amygdala connectivity to brain areas involved in executive control may underlie these limited abilities during adolescence.

SUBMITTER: Ravindranath O

PROVIDER: S-EPMC7451790 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Influences of affective context on amygdala functional connectivity during cognitive control from adolescence through adulthood.

Ravindranath Orma O Ordaz Sarah J SJ Padmanabhan Aarthi A Foran William W Jalbrzikowski Maria M Calabro Finnegan J FJ Luna Beatriz B

Developmental cognitive neuroscience 20200814

Emotion processing is believed to dominate over other brain functions during adolescence, including inhibitory control. However, few studies have examined the neural underpinnings of affective states during cognitive control. Here, we characterized the brain in an affective state by cross-sectionally assessing age-related changes in amygdala background connectivity during an affective inhibitory control task. Participants completed an antisaccade (AS) fMRI task while affective auditory stimuli w ...[more]

PMID: 32836077

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Project description:BACKGROUND: Motivational and cognitive abnormalities are frequently reported in pathological gambling. However, studies simultaneously investigating motivational and cognitive processing in problematic gamblers are lacking, limiting our understanding of the interplay between these systems in problematic gambling. Studies in non-clinical samples indicate that interactions between dorsal "executive" and ventral "affective" processing systems are necessary for adequate responses in various emotive situations. METHODS: We conducted a generalized Psycho-Physiological Interaction (gPPI) analysis to assess the influence of affective stimuli on changes in functional connectivity associated with response inhibition in 16 treatment seeking problematic gamblers (PRGs) and 15 healthy controls (HCs) using an affective Go-NoGo fMRI paradigm including neutral, gambling-related, positive and negative pictures as neutral and affective conditions. RESULTS: Across groups, task performance accuracy during neutral inhibition trials was positively correlated with functional connectivity between the left caudate and the right middle frontal cortex. During inhibition in the gambling condition, only in PRGs accuracy of task performance was positively correlated with functional connectivity within sub-regions of the dorsal executive system. Group interactions showed that during neutral inhibition, HCs exhibited greater functional connectivity between the left caudate and occipital cortex than PRGs. In contrast, during inhibition in the positive condition, PRGs compared to HCs showed greater functional connectivity between the left caudate and occipital cortex. During inhibition trials in the negative condition, a stronger functional connectivity between the left caudate and the right anterior cingulate cortex in PRGs compared to HCs was present. There were no group interactions during inhibition in the gambling condition. CONCLUSIONS: During gamble inhibition PRGs seem to benefit more from functional connectivity within the dorsal executive system than HCs, because task accuracy in this condition in PRGs is positively correlated with functional connectivity, although the groups show similar connectivity patterns during gamble inhibition. Greater functional connectivity between the ventral affective system and the dorsal executive system in PRGs in the affective conditions compared to HCs, suggests facilitation of the dorsal executive system when affective stimuli are present specifically in PRGs.

Project description:BackgroundExternalizing behavior has been attributed, in part, to decreased frontolimbic control over amygdala activation. However, little is known about developmental trajectories of frontoamygdalar functional connectivity and its relation to externalizing behavior. The present study addresses this gap by examining longitudinal associations between adolescent and adult externalizing behavior and amygdala-anterior cingulate cortex (ACC) and amygdala-orbitofrontal cortex (OFC) resting-state functional connectivity in a sample of 111 typically developing participants aged 11-23 at baseline.MethodsParticipants completed two-to-four data waves spaced approximately two years apart, resulting in a total of 309 data points. At each data wave, externalizing behavior was measured using the Externalizing Behavior Broadband Scale from the Achenbach Youth/Adult Self-Report questionnaire. Resting-state fMRI preprocessing was performed using FSL. Amygdala functional connectivity was examined using AFNI. The longitudinal association between externalizing behavior and amygdala-ACC/OFC functional connectivity was examined using linear mixed effect models in R.ResultsExternalizing behavior was associated with increased amygdala-ACC and amygdala-OFC resting-state functional connectivity across adolescence and young adulthood. For amygdala-ACC connectivity, externalizing behavior at baseline primarily drove this association, whereas for amygdala-OFC functional connectivity, change in externalizing behavior relative to baseline drove the main effect of externalizing behavior on amygdala-OFC functional connectivity. No evidence was found for differential developmental trajectories of frontoamygdalar connectivity for different levels of externalizing behavior (i.e., age-by-externalizing behavior interaction effect).ConclusionsHigher externalizing behavior is associated with increased resting-state attunement between the amygdala and ACC/OFC, perhaps indicating a generally more vigilant state for neural networks important for emotional processing and control.

Dataset Information

Influences of affective context on amygdala functional connectivity during cognitive control from adolescence through adulthood.

Publications

Influences of affective context on amygdala functional connectivity during cognitive control from adolescence through adulthood.

Similar Datasets

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