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Increased left inferior fronto-striatal activation during error monitoring after fMRI neurofeedback of right inferior frontal cortex in adolescents with attention deficit hyperactivity disorder.

ABSTRACT: Attention Deficit/Hyperactivity Disorder (ADHD) is a self-regulation disorder, with impairments in error monitoring associated with underactivation of the related brain network(s). Psychostimulant medication improves ADHD symptoms and can upregulate brain function, but has side effects, with limited evidence for longer-term effects. Real-time functional magnetic resonance neurofeedback (fMRI-NF) has potential longer-term neuroplastic effects. We previously reported the effects of 11 runs of 8.5 min of fMRI-NF of the right inferior frontal cortex (rIFC) in adolescents with ADHD. This resulted in improvement of clinical symptom and enhanced rIFC activation post-pre treatment during response inhibition, when compared to a control group receiving fMRI-NF of the left parahippocampal gyrus (lPHG). In the current study we applied a novel analysis to the existing data by investigating the effects of fMRI-NF of rIFC in 16 adolescents with ADHD compared to fMRI-NF of lPHG in 11 adolescents with ADHD on the neurofunctional correlates of error monitoring during the same fMRI tracking stop task and potential associations with cognitive and clinical measures. We found stronger performance adjustment to errors in the rIFC-NF compared to the control lPHG-NF group. At the brain function level, fMRI-NF of rIFC compared to that of lPHG was associated with increased activation in error monitoring regions of the left IFC, premotor cortex, insula and putamen. The increased activation in left IFC-insular-striatal error monitoring regions in the rIFC-NF relative to the lPHG-NF group was furthermore trend-wise correlated with NF-induced ADHD symptom improvements. The findings of this study show, that during error monitoring, fMRI-NF training of rIFC upregulation elicited improvement in post-error behavioural adjustments and concomitant increased activation in left hemispheric fronto-insular-striatal and premotor regions mediating self-control and self-monitoring functions. This suggests that the administration of fMRI-NF of the rIFC may have had an impact on wider networks of self-regulation and self-monitoring in adolescents with ADHD.

SUBMITTER: Criaud M

PROVIDER: S-EPMC7306625 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Increased left inferior fronto-striatal activation during error monitoring after fMRI neurofeedback of right inferior frontal cortex in adolescents with attention deficit hyperactivity disorder.

Criaud M M Wulff M M Alegria A A AA Barker G J GJ Giampietro V V Rubia K K

NeuroImage. Clinical 20200610

Attention Deficit/Hyperactivity Disorder (ADHD) is a self-regulation disorder, with impairments in error monitoring associated with underactivation of the related brain network(s). Psychostimulant medication improves ADHD symptoms and can upregulate brain function, but has side effects, with limited evidence for longer-term effects. Real-time functional magnetic resonance neurofeedback (fMRI-NF) has potential longer-term neuroplastic effects. We previously reported the effects of 11 runs of 8.5 ...[more]

PMID: 32570204

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Project description:Functional Magnetic Resonance Imaging Neurofeedback (fMRI-NF) targeting brain areas/networks shown to be dysfunctional by previous fMRI research is a promising novel neurotherapy for ADHD. Our pioneering study in 31 adolescents with ADHD showed that fMRI-NF of the right inferior frontal cortex (rIFC) and of the left parahippocampal gyrus (lPHG) was associated with clinical improvements. Previous studies using electro-encephalography-NF have shown, however, that not all ADHD patients learn to self-regulate, and the predictors of fMRI-NF self-regulation learning are not presently known. The aim of the current study was therefore to elucidate the potential predictors of fMRI-NF learning by investigating the relationship between fMRI-NF learning and baseline inhibitory brain function during an fMRI stop task, along with clinical and cognitive measures. fMRI-NF learning capacity was calculated for each participant by correlating the number of completed fMRI-NF runs with brain activation in their respective target regions from each run (rIFC or lPHG); higher correlation values were taken as a marker of better (linear) fMRI-NF learning. Linear correlations were then conducted between baseline measures and the participants' capacity for fMRI-NF learning. Better fMRI-NF learning was related to increased activation in left inferior fronto-striatal regions during the fMRI stop task. Poorer self-regulation during fMRI-NF training was associated with enhanced activation in posterior temporo-occipital and cerebellar regions. Cognitive and clinical measures were not associated with general fMRI-NF learning across all participants. A categorical analysis showed that 48% of adolescents with ADHD successfully learned fMRI-NF and this was also not associated with any baseline clinical or cognitive measures except that faster processing speed during inhibition and attention tasks predicted learning. Taken together, the findings suggest that imaging data are more predictive of fMRI-NF self-regulation skills in ADHD than behavioural data. Stronger baseline activation in fronto-striatal cognitive control regions predicts better fMRI-NF learning in ADHD.

Dataset Information

Increased left inferior fronto-striatal activation during error monitoring after fMRI neurofeedback of right inferior frontal cortex in adolescents with attention deficit hyperactivity disorder.

Publications

Increased left inferior fronto-striatal activation during error monitoring after fMRI neurofeedback of right inferior frontal cortex in adolescents with attention deficit hyperactivity disorder.

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