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Adolescent sex differences in cortico-subcortical functional connectivity during response inhibition.

ABSTRACT: Numerous lines of evidence have shown that cognitive processes engaged during response inhibition tasks are associated with structure and functional integration of regions within fronto-parietal networks. However, while prior studies have started to characterize how intrinsic connectivity during resting state differs between boys and girls, comparatively less is known about how functional connectivity differs between males and females when brain function is exogenously driven by the processing demands of typical Go/No-Go tasks that assess both response inhibition and error processing. The purpose of this study was to characterize adolescent sex differences and possible changes in sexually dimorphic regional functional connectivity across adolescent development in both cortical and subcortical brain connectivity elicited during a visual Go/No-Go task. A total of 130 healthy adolescents (ages 12-25 years) performed a Go/No-Go task during functional magnetic resonance imaging. High model-order group independent component analysis was used to characterize whole-brain network functional connectivity during response inhibition and then a univariate technique used to evaluate differences related to sex and age. As predicted and similar to previously described findings from non-task-driven resting state connectivity studies, functional connectivity sex differences were observed in several subcortical regions, including the amygdala, caudate, thalamus, and cortical regions, including inferior frontal gyrus engaged most strongly during successful response inhibition and/or error processing. Importantly, adolescent boys and girls exhibited different normative profiles of age-related changes in several default mode networks of regions and anterior cingulate cortex. These results suggest that cortical-subcortical functional networks supporting response inhibition operate differently between sexes during adolescence.

SUBMITTER: Chung YS

PROVIDER: S-EPMC8259338 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAttention-deficit/hyperactivity disorder (ADHD) is associated with atypical fronto-subcortical neural circuitry and heightened delay discounting, or a stronger preference for smaller, immediate rewards over larger, delayed rewards. Recent evidence of ADHD-related sex differences in brain structure and function suggests anomalies in fronto-subcortical circuitry may differ among girls and boys with ADHD. The current study examined whether the functional connectivity (FC) within fronto-subcortical neural circuitry differs among girls and boys with ADHD compared to same-sex typically developing (TD) controls and relates to delay discounting.MethodsParticipants include 8-12-year-old children with ADHD (n?=?72, 20 girls) and TD controls (n?=?75, 21 girls). Fronto-subcortical regions of interest were functionally defined by applying independent component analysis to resting-state fMRI data. Intrinsic FC between subcortical components, including the striatum and amygdala, and prefrontal components, including ventromedial prefrontal cortex (vmPFC), anterior cingulate cortex (ACC), and anterior dorsolateral prefrontal cortex (dlPFC), was compared across diagnostic groups overall and within sex. Correlations between intrinsic FC of the six fronto-subcortical pairs and delay discounting were also examined.ResultsBoth girls and boys with ADHD show atypical FC between vmPFC and subcortical regions including the striatum (stronger positive FC in ADHD) and amygdala (weaker negative FC in ADHD), with the greatest diagnostic effects among girls. In addition, girls with ADHD show atypical intrinsic FC between the striatum and dlPFC components, including stronger positive FC with ACC and stronger negative FC with dlPFC. Further, girls but not boys, with ADHD, show heightened real-time delay discounting. Brain-behavior correlations suggest (1) stronger negative FC between the striatal and dlPFC components correlated with greater money delay discounting across all participants and (2) stronger FC between the amygdala with both the dlPFC and ACC components was differentially related to heightened real-time discounting among girls and boys with and without ADHD.ConclusionsOur findings suggest fronto-subcortical functional networks are affected in children with ADHD, particularly girls, and relate to delay discounting. These results also provide preliminary evidence of greater disruptions in fronto-subcortical FC among girls with ADHD that is not due to elevated inattention symptom severity, intellectual reasoning ability, age, or head motion.

Project description:BackgroundMany patients with attention-deficit/hyperactivity disorder (ADHD) display aberrant reward-related behavior. Task-based fMRI studies have related atypical reward processing in ADHD to altered BOLD activity in regions underlying reward processing such as ventral striatum and orbitofrontal cortex. However, it remains unclear whether the observed effects are region-specific or related to changes in functional connectivity of networks supporting reward processing. Here we use resting-state fMRI to comprehensively delineate the functional connectivity architecture underlying aberrant reward processing in ADHD.MethodsWe assessed resting-state functional connectivity of four networks that support reward processing. These networks showed high spatial overlap with the default mode, fronto-parietal, lateral visual, and salience networks, yet only activity within the salience network was effectively sensitive to reward value. We parcelled these networks into their functional cortical and subcortical subregions and obtained functional connectivity matrices by computing Pearson correlations between the regional time series. We compared functional connectivity within each of the four networks between participants with ADHD and controls, and related functional connectivity to dimensional ADHD symptom scores across all participants (N = 444; age range: 8.5-30.5; mean age: 17.7).ResultsWe did not observe significant ADHD-related alterations in functional connectivity of the salience network, which included key reward regions. Instead, levels of inattention symptoms modulated functional connectivity of the default-mode and fronto-parietal networks, which supported general task processing.ConclusionsThe present study does not corroborate previous childhood evidence for functional connectivity alterations between key reward processing regions in adolescents and young adults with ADHD. Our findings could point to developmental normalization or indicate that reward-processing deficits result from functional connectivity alterations in general task-related networks.

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Adolescent sex differences in cortico-subcortical functional connectivity during response inhibition.

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