Abstract
A brain-computer-interface (BCI)-based attention training game system has shown promise for treating attention deficit/hyperactivity disorder (ADHD) children with inattentive symptoms. However, little is known about brain network organizational changes underlying behavior improvement following BCI-based training. To cover this gap, we aimed to examine the topological alterations of large-scale brain functional networks induced by the 8-week BCI-based attention intervention in ADHD boys using resting-state functional magnetic resonance imaging method. Compared to the non-intervention (ADHD-NI) group, the intervention group (ADHD-I) showed greater reduction of inattention symptoms accompanied with differential brain network reorganizations after training. Specifically, the ADHD-NI group had increased functional connectivity (FC) within the salience/ventral attention network (SVN) and increased FC between task-positive networks (including the SVN, dorsal attention (DAN), somatomotor, and executive control network) and subcortical regions; in contrast ADHD-I group did not have this pattern. In parallel, ADHD-I group had reduced degree centrality and clustering coefficient as well as increased closeness in task-positive and the default mode networks (prefrontal regions) after the training. More importantly, these reduced local functional processing mainly in the SVN were associated with less inattentive/internalizing problems after 8-week BCI-based intervention across ADHD patients. Our findings suggest that the BCI-based attention training facilitates behavioral improvement in ADHD children by reorganizing brain functional network from more regular to more random configurations, particularly renormalizing salience network processing. Future long-term longitudinal neuroimaging studies are needed to develop the BCI-based intervention approach to promote brain maturation in ADHD.
Highlights
Attention deficit/hyperactivity disorder (ADHD) is one of the most commonly diagnosed neuropsychiatric disorders of childhood affecting 3–10% of children[1]
We found significant group and time interaction in the functional connectivity (FC) within the salience/ventral attention network (SVN) (p = 0.019) and between the SVN and dorsal attention networks (DAN) (p = 0.035), SVN and SMN (p = 0.014), SVN and subcortical network (p = 0.050), and SMN and ECN (p = 0.049, Fig. 3b, Supplementary Table 2), which indicated a trend of ADHD-NI group having increased FC within the SVN and between the SVN with DAN and other networks over time while ADHD-I did not exhibit this pattern
Among the FC measures showing significant time and group effect, we found that less increase of FC in the intra-SVN and the inter-network between SVN and DAN resulted in more behavior improvement of the internalizing problems in children with ADHD (r = 0.41, p = 0.028 and r = 0.38, p = 0.040, respectively; Fig. 3c, d)
Summary
Attention deficit/hyperactivity disorder (ADHD) is one of the most commonly diagnosed neuropsychiatric disorders of childhood affecting 3–10% of children[1]. Medications used to treat ADHD such as methylphenidate, amphetamine, and atomoxetine indicate a dopamine/norepinephrine deficit as the neurochemical basis of ADHD, but the etiology is more complex. These agents have poor adverse effect profiles and a multitude of drug interactions[4]. A few studies hypothesized that brain-computer-interface (BCI)-based neurofeedback system using specific EEG signals could induce neuroplastic changes in nervous systems[9,10] Following this hypothesis, a BCI-based attention training game system was designed for treating ADHD children with significant inattentive symptoms[11]. The treatment effects of such neurofeedback-based training in children with ADHD were thought to relate to the successful regulation of brain activity and the ability of the brain to change and adapt, known as brain plasticity[8,9]
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