Behavioral Consequences of Aberrant Alpha Lateralization in Attention-Deficit/Hyperactivity Disorder

doi:10.1016/j.biopsych.2013.02.001

Biological Psychiatry

Volume 74, Issue 3, 1 August 2013, Pages 227-233

https://doi.org/10.1016/j.biopsych.2013.02.001 Get rights and content

Background

Attention-deficit/hyperactivity disorder (ADHD) is characterized by problems in directing and sustaining attention. Recent findings suggest that alpha oscillations (8–12 Hz) are crucially involved in gating information between brain regions when allocating attention. The current study investigates whether aberrant modulation of alpha oscillations contributes to attention problems in ADHD patients.

Methods

Magnetoencephalographic signals were recorded in adults with ADHD (n = 17) and healthy control subjects (n = 18) while they performed a visuospatial attention task. Cues directed attention to the left or right visual hemifield with an 80% validity with respect to the upcoming target.

Results

Unlike the control group, subjects with ADHD showed a higher accuracy for invalidly cued right targets compared with invalidly cued left targets (p = .04). This coincided with an inability of the ADHD subjects to sustain the posterior hemispheric alpha lateralization in the period before the target for the left cue condition (p = .011). Furthermore, the control group showed a strong correlation between the degree of alpha lateralization and the magnitude of the cueing effect assessed in terms of accuracy (r_s = .71, p = .001) and reaction times (r_s =−.81, p<.001). These correlations were absent in the ADHD group.

Conclusions

Our results demonstrate that subjects with ADHD have a failure in sustaining hemispheric alpha lateralization when cued to the left, resulting in an attentional bias to the right visual hemifield. These findings suggest that aberrant modulations of alpha oscillations reflect attention problems in ADHD and might be related to the neurophysiological substrate of the disorder.

Section snippets

Subjects

A total of 41 adults (ages 21–40 years) were recruited for this study from an existing database of adult ADHD patients and healthy control subjects (Dutch cohort of the IMpACT [International Multicenter Persistent ADHD Collaboration] study) (28). Participants included adult ADHD patients (n = 17) and IQ-, age-, and gender-matched healthy control subjects (n = 18). Six subjects (two ADHD patients, four control subjects) were not included in the final data analysis for reasons described in the

Results

No significant difference was found on demographic variables, other than the scores for the ADHD self-report, which were significantly higher in the ADHD group compared with the control group (p<.001) (Table 1). The MEG data were acquired from both groups performing the spatial-cueing paradigm described in Figure 1. The total number of trials after rejecting data with artefacts or eye movements did not differ between the groups (control subjects: 718±138; ADHD: 721±108; p = .94; independent

Discussion

The current study addresses the question of whether attention deficits in ADHD are associated with problems in modulating alpha oscillations. To elicit hemispheric lateralization of posterior alpha activity, a motion coherence detection task was used in which subjects were instructed to covertly attend to either the left or the right visual field. Analyses of performance and simultaneous MEG recordings of brain activity revealed remarkable differences when comparing the ADHD and control group

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In the present study, 8−13-year-old children with ADHD also showed significant alpha lateralization during the early stage of cue maintenance. However, alpha lateralization decreased rapidly during the late stage of cue maintenance, and this dysfunctional sustainable alpha modulation in childhood might not be corrected even in adulthood in patients with ADHD (Hale et al., 2015; ter Huurne et al., 2013; Hale et al., 2010; Hale et al., 2009b). N2pc is an individuated representation and neurophysiological marker of attentional selection that is sensitive to development (Foster et al., 2020; Ester et al., 2012; Drew and Vogel, 2008; Luck and Hillyard, 1994a, 1994b; Eimer, 1996).
Attention-deficit/hyperactivity disorder (ADHD) is characterized by attention problems. The current study investigated whether and how anticipatory alpha oscillations, the subsequent target-elicited N2 posterior-contralateral component (N2pc) and their relationship contributed to attention problems in children with ADHD.
Electroencephalograms (EEGs) were recorded from 8−13-year-old children with ADHD and typically developing children during a cued visuospatial covert attention task.
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Previous studies have found that theta activities exhibit posterior lateralized modulation as well as midfrontal event-related synchronization (ERS) during covert visual attention in adults. The present study investigated whether these theta modulations existed in children and whether they were associated with attentional problems in attention-deficit/hyperactivity disorder (ADHD). Electroencephalography signals were recorded from typically developing (TD) children and children with ADHD (TD: n = 24; ADHD: n = 22) while they performed a cued covert visual attention task. The participants responded to a target following a cue designed as human eyes that gazed to the left or right visual field (70% validity). Compared with the TD children, the children with ADHD showed increased midfrontal theta ERS and significant posterior theta lateralization in response to the cues. More importantly, we found that the stronger posterior theta lateralization in the right hemisphere exhibited a positive trial-based correlation with the larger midfrontal theta ERS and predicted lower RT variability at the trial level in the children with ADHD. We suggest that ADHD may be associated with some enhanced systems in the frontal and posterior areas via theta oscillations, which may be involved in the compensatory maturation for their attention deficits in childhood, thereby promoting the stability of behavioral responses.

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Archival ReportBehavioral Consequences of Aberrant Alpha Lateralization in Attention-Deficit/Hyperactivity Disorder

Background

Methods

Results

Conclusions

Section snippets

Subjects

Results

Discussion

Brain Res Cogn Brain Res

Brain Res Cogn Brain Res

Neuroimage

Neuron

Brain Res Rev

Brain Res Rev

Trends Cogn Sci

Trends Cogn Sci

Clin Neurophysiol

Biol Psychiatry

Neuropsychologia

Clin Neurophysiol

Neuropsychologia

Brain Cogn

Neuropsychologia

Neuropsychologia

Neuropsychologia

Diagnostic and Statistical Manual of Mental Disorders

Text Rev

Cross-national prevalence and correlates of adult attention-deficit hyperactivity disorder

Br J Psychiatry

The worldwide prevalence of ADHD: A systematic review and metaregression analysis

Am J Psychiatry

The attention system of the human brain

Annu Rev Neurosci

Parieto-occipital approximately 10 Hz activity reflects anticipatory state of visual attention mechanisms

Neuroreport

Anticipatory biasing of visuospatial attention indexed by retinotopically specific alpha-band electroencephalography increases over occipital cortex

J Neurosci

A shift of visual spatial attention is selectively associated with human EEG alpha activity

Eur J Neurosci

Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention

J Neurophysiol

Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection

J Neurosci

Archival Report
Behavioral Consequences of Aberrant Alpha Lateralization in Attention-Deficit/Hyperactivity Disorder