Executive functions are a series of interrelated higher-order cognitive processes that control goal-directed behavior and problem-solving (Miyake et al. 2000). This study found that children with ADHD showed more executive functioning deficits, thus supporting Barkley’s model (Kofler et al. 2010). Executive dysfunction may represent an important target for preventing functional impairment in multiple domains in children with ADHD. Therefore, we investigated the neuropathological mechanisms underlying ADHD using EEG.
The study of functional brain connectivity contributes to our understanding of the neural mechanisms of ADHD and can reveal patterns of brain network connectivity that are dysregulated in patients with ADHD. In the present study, we found that children with ADHD had diminished connectivity between the frontal and parietal regions in the beta band and between the frontal regions in the gamma band in both the closed- and open-eye states compared with the HC group. Robbie et al. (2016) found that children with ADHD display reduced coherence in different regions of the cerebral hemispheres. The executive control network, comprising the supraparietal and prefrontal lobes, thalamus, and striatum, is a hotspot in the study of functional brain networks in ADHD. Previous structural magnetic resonance imaging (MRI) studies have found reduced frontal and dorsolateral prefrontal volumes and significantly thinner cortices in patients with ADHD, which have been associated with the severity of hyperactivity/impulsivity and cognitive deficits (Shaw et al. 2011; Proal et al. 2011). Additionally, functional MRI (fMRI) studies have shown reduced activation of the superior parietal gyrus and left dorsolateral prefrontal cortical regions of the brain in children with ADHD when performing attention-related vigilance tasks (Christakou et al. 2013). Similarly, fMRI studies have demonstrated reduced activation of the superior parietal gyrus and left dorsolateral prefrontal cortical regions of the brain in children with ADHD when performing inhibitory control tasks (Christakou et al. 2013). Children with ADHD show hypoactivation of the left superior frontal lobe when performing tasks of inhibitory control (Hwang et al. 2019). We suggest that executive function and attention dysfunction in children with ADHD may be related to abnormal functional connectivity between the aforementioned brain regions. Children with ADHD have reduced activation of their executive control networks in both task and resting states and can experience functional impairments in impulsivity, oppositional behavior, response inhibition, and attentional control. Patients with ADHD have abnormally low presynaptic dopamine stores in the prefrontal cortex, severely impairing attentional function, cognitive processes, and working memory (Kollins and Adcock 2014). The prefrontal-cerebellar circuit undergoes core dysfunction in patients with ADHD, and its functional connectivity may underlie the neural basis of multidimensional behavioral deficits closely related to the manifestation of syndromic symptoms (Durston et al. 2011). Bakhshi et al. (2022) found that the frontocerebellar circuits of patients with ADHD had different ratios of choline/creatine and glutamate/creatine and that alterations in frontal-cerebellar metabolites may be related to cognitive and behavioral deficits. Altered EEG coherence suggests that functional connectivity between brain regions can provide important information about brain activation and neuropsychological features. In addition to prefrontal cortical activation, coherent patterns in frontal-parietal regions play a crucial role in executive function (Van Son et al. 2019). Many studies, including fMRI and EEG, have emphasized that the most common cognitive deficits in patients with ADHD are related to frontal or parietal cortical dysfunction and that abnormal EEG may be a good predictor of cognitive impairment in ADHD (Hoogman et al. 2017). The present study found reduced functional connectivity in the frontoparietal regions of the beta and gamma frequency bands, suggesting that this may be related to executive function abnormalities in children with ADHD. The neural mechanisms in patients with ADHD may involve localized functional abnormalities in the frontal and parietal brain regions. A reduction in internal connectivity between the frontal and parietal regions may be the neurological basis for the symptoms of ADHD and abnormalities in executive functions.
We analyzed resting-state EEG data from patients with ADHD and healthy children and used graph theory to help understand the possible neural mechanisms of ADHD from the perspective of functional networks, contributing to the understanding of the pathogenesis of ADHD. In the present study, we found diminished frontal- and parietal-dominated connectivity only in the beta and gamma bands when comparing the ADHD and HC groups, and abnormal alterations in network parameter analyses were found only in the beta band. In children with ADHD, CPL decreased in the eyes-closed state, whereas the GE increased and the CPL, CC, and LE decreased in the eyes-open state. Brain networks in children with ADHD have problems transferring information between different neural regions, and the beta band better reflects the differences between children with ADHD and HCs and may be the best EEG sub-band to investigate connectivity impairments in ADHD (Michelini et al. 2019). In this study, CPL was lower in the ADHD group than in the HC group, suggesting that information is more aggregated in the brains of children with ADHD than in healthy children and that this aggregation impedes the easy transfer of information (Dini et al. 2020). Patients with ADHD are more likely to have elevated GE in early childhood, and an elevated GE reflects overactive functional integration, which may disrupt the transfer of information across the entire brain and impede complex cognitive functions (Ma et al. 2018; Furlong et al. 2021). A higher CC indicates a more complex information exchange between brain regions (Fornito et al. 2015), which may lead to increased susceptibility to ADHD. This study found reduced CC in children with ADHD, which may be related to the heterogeneity and variability of brain activity in these children. The reduced LE in children with ADHD in this study suggests reduced functional separation of local brain regions. In complex networks, shorter path lengths are not necessarily advantageous, and lower CC and CPL imply a faster transition to network randomness (De Haan et al. 2009).
There is a correlation between executive function and topological properties in patients with ADHD (Zhou et al. 2023), and these properties may reflect differences in neural network patterns between the disorders. In this study, anxiety in BRIEF2 and LE were positively correlated in the beta band with eyes closed, and emotional control and CRI were positively correlated with both CC and LE in the gamma band. In the beta band of the eyes-open state, emotional control in BRIEF2 was positively correlated with CC and LE. It has been suggested that the more pronounced the executive function symptoms in children with ADHD, the lower the ability of brain networks to transmit information to each other. Previous studies have shown that 35% of children with ADHD exhibit extensive deficits in multiple domains of executive functioning, and 89% of children with ADHD exhibit objectively defined impairments in at least one executive function, findings that suggest substantial heterogeneity in executive functioning deficits in individuals with ADHD (Kofler et al. 2019). Cognitive function is an important intermediate phenotype connecting the brain and behavioral performance and is a potential factor explaining the heterogeneity of ADHD (Tripp and Wickens 2009). Executive function impairments have been linked to underlying neural mechanisms. A meta-analysis of task-state MRI involving executive function showed that patients with ADHD exhibited reduced activation of the frontoparietal network (Cortese et al. 2012).
Our study did have some limitations: Although this study had a large sample size, the number of female patients included was still small. Future studies need to increase the sample size of female patients to help compare differences in EEG characteristics between sexes. EEG signals have a high temporal resolution, but their spatial resolution is limited. In the future, multiple functional brain imaging techniques can be jointly applied to combine the high spatial resolution of brain imaging with the high temporal resolution of EEG signals to obtain more reliable neural network features.
In summary, we identified local functional abnormalities in the frontal and parietal brain regions in the pathogenesis of ADHD in children based on EEG data through the construction of a functional brain network. Children’s brain networks have problems transmitting information between different neural regions, which may lead to the development of the disease, with the beta band reflecting differences between the two groups of children. Impairment in the executive function of children with ADHD reflects underlying neurological mechanisms. Our findings offer potential for identifying neural markers of ADHD through EEG network analysis. Future studies are required to investigate the clinical utility of this approach for diagnosis and to develop targeted interventions aimed at improving information flow within these dysfunctional networks in ADHD.