Attention deficit hyperactivity disorder (ADHD) is a common neurodevelopmental disease in school age children. Some studies found that children with ADHD showed an impairment and poor behavioural performance in visual selective attention tasks. Previous studies have found that alpha oscillations in the parietooccipital area are significantly modulated in goal-directed (cue-related) orienting and target-induced selective attention, which shows that the parietooccipital alpha oscillations not only reflect the process of active attention orienting, but also reflect the neural activities related to the processing of target features. In ADHD research, although cue-related posterior alpha modulation has been widely studied, none of the published studies have examined target-induced posterior alpha modulation during visual search in patients with ADHD. In addition, theta oscillations in the midfrontal area reflect the neural mechanism related to cognitive control. When people actively focus their attention on certain objects or features, the midfrontal theta and posterior alpha oscillations show significant functional connectivity, while the connectivity in children with ADHD was significantly lower than that typically developing (TD) children.
In March 2022, the journal, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, published a paper entitled “Abnormal reactivity of brain oscillations to visual search target in children with attention-deficit/hyperactivity disorder” by Prof. Yan Song’s research team at the State Key Laboratory of Cognitive Neuroscience and Learning of Beijing Normal University. Using a classical visual search task (Figure 1), the study investigated the midfrontal theta Event-related synchronization (ERS) of the midfrontal theta oscillations and the lateralized modulation of the parieto-occipital alpha oscillations during target selection in TD children (n = 72) and children with ADHD (n = 96).
Figure 1. Visual search array and behavioral results.
The study found that TD children and children with ADHD showed significant midfrontal theta ERS and parietooccipital alpha modulation in the visual search task. Compared with TD children, children with ADHD showed lower midfrontal theta ERS and higher alpha lateralized modulation in the parietooccipital area (as shown in Figure 2).
Figure 2. Midfrontal theta ERS and parietooccipital alpha modulation in TD and ADHD groups.
In this study, trial-based Spearman correlation coefficient was used to describe the connectivity between frontal theta ERS and posterior alpha modulation. The results showed that TD children showed a significant positive correlation between midfrontal theta ERS and posterior alpha modulation, while children with ADHD did not show this feature (as shown in Figure 3).
Figure 3. The trial-based correlation coefficients between the averaged midfrontal theta ERS (250–600 ms) and the posterior alpha lateralization index (LI).
Trial-based Spearman correlation coefficient was used to describe the correlation between EEG indexes (theta ERS and alpha modulation index) and behavioral indicators (reaction time (RT) and RT variability (RTV)). The results showed that midfrontal theta ERS in TD children showed a significant negative correlation with RTV, but this feature was absent in children with ADHD. The correlation coefficient of TD children was significantly lower than that of children with ADHD (as shown in Figure 4).
Figure 4. The trial-based correlation coefficients between the EEG indexes (theta ERS and alpha LI) and behavioural indicators (RT and RTV).
The decrease of midfrontal theta ERS induced by visual search target in children with ADHD suggests that the lack of executive control ability may become a limiting factor of visual spatial attention under the condition that more executive control resources are needed. The decrease of midfrontal theta ERS in children with ADHD may reflect the characteristics of insufficient executive control in the process of visual search, which is considered to be one of core defects of ADHD.
Correlation analyses showed that the improvement of theta ERS effectively promoted the stability of behavioral response in TD children, but not in ADHD group, which indicates that the frontal network plays an important role in maintaining behavioral stability, and the weakening of midfrontal theta wave activity may be an important factor affecting the behavioral pattern of children with ADHD.
This study first found target-induced posterior alpha lateralization in the visual search process in a child population. A previous study on healthy adults indicated that target-induced alpha lateralization existed only under the condition when the target was paired with a low-similarity (colour) distractor, which is interpreted as a mechanism related to feature extraction and processing of the target. However, in this study, children still showed significant posterior alpha lateralization in a visual search task in which the colour of the target was the same as irrelevant stimuli. The authors speculate that because the neurobiological systems involved in visual processing and attention selection is still maturing in children, children may voluntarily recruit additional attentional resources to select the target features, which increases posterior alpha lateralization. Children with ADHD experience difficulty recruiting sufficient attentional control resources to complete the visual search task with interference stimuli, and the excessive alpha lateralization in children with ADHD may reflect the functional compensation of attention networks for the deficits in visual attention.
In this study, the most important finding is the positive connection between midfrontal theta ERS and parietooccipital alpha modulation during target selection in TD children, which is not shown in children with ADHD. This is consistent with previous findings that the functional connection between midfrontal theta and the posterior alpha oscillations in ADHD patients is weakened during the cue indicating stage. The cross-frequency connection in TD children might reflect a form of a top-down effect of the frontal executive control systems on the perceptual structures in the parieto-occipital area, which are involved in active target processing. The diminished correlation in children with ADHD might reflect the lack of top-down cognitive control over the posterior alpha oscillations, which play a role in the gating of target information.
From the above findings, it can be seen that children with ADHD show different brain oscillation characteristics between cue-directed attention orientation and visual search processes. This suggests that ADHD patients may have two different neural activities related to the two types of attention: visual attention deficit and functional compensation. These findings provide novel evidence for explaining the developmental characteristics of visual attention in children with ADHD.
This study is the expansion and continuation of researches of Yan Song's team on visual attention mechanism of attention development and ADHD in children (Wang et al., 2016, 2017; sun et al., 2018; Guo et al., 2019, 2020; Luo et al., 2021). The first author is Jialiang Guo, postdoctoral of Beijing Normal University, the second author is Xiangsheng Luo, doctoral student of the Sixth Hospital of Peking University, the third and fourth authors are Yuanjun Kong and Bingkun Li, doctoral students of Beijing Normal University, and the corresponding authors are Professor Yan Song of Beijing Normal University and Professor Li Sun of the Sixth Hospital of Peking University. Thank Professor Bailu Si of Beijing Normal University for his guidance and help to this study. The research was supported by the National Natural Science Foundation of China.
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