Functional Disconnection of Frontal Cortex and Visual Cortex in Attention-Deficit/Hyperactivity Disorder

doi:10.1016/j.biopsych.2009.11.022

Biological Psychiatry

Volume 67, Issue 7, 1 April 2010, Pages 617-623

https://doi.org/10.1016/j.biopsych.2009.11.022 Get rights and content

Background

Current pathophysiologic models of attention-deficit/hyperactivity disorder (ADHD) suggest that impaired functional connectivity within brain attention networks may contribute to the disorder. In this electroencephalographic (EEG) study, we analyzed cross-frequency amplitude correlations to investigate differences in cue-induced functional connectivity in typically developing children and children with ADHD.

Methods

Electroencephalographic activity was recorded in 25 children aged 8 to 12 years (14 with ADHD) while they performed a cross-modal attention task in which cues signaled the most likely (.75 probability) modality of an upcoming target. The power spectra of the EEG in the theta (3–5 Hz) and alpha (8–12 Hz) bands were calculated for the 1-sec interval after the cue and before the target while subjects prepared to discriminate the expected target.

Results

Both groups showed behavioral benefits of the predictive attentional cues, being faster and more accurate for validly cued targets (e.g., visual target preceded by a cue predicting a visual target) than to invalidly cued targets (e.g., visual target preceded by a cue predicting an auditory target); in addition, independent of cue-target validity, typical children were faster to respond overall. In the typically developing children, the alpha activity was differentially modulated by the two cues and anticorrelated with midfrontal theta activity; these EEG correlates of attentional control were not observed in the children with ADHD.

Conclusions

Our findings provide neurophysiological evidence for a specific deficit in top-down attentional control in children with ADHD that is manifested as a functional disconnection between frontal and occipital cortex.

Section snippets

Subjects and Inclusion Criteria

Children aged 8 to 12 years with typical development or ADHD-combined type were enrolled following informed written parental consent. The inclusion criteria for typically developing children was that, based on parent interview, they be free from neurodevelopmental disorders, including autism spectrum disorder and ADHD, using the Diagnostic Interview Schedule for Children, and that they be unrelated to the ADHD children. The inclusion criteria for the ADHD-combined type were as follows. The

Behavioral Data

Overall, independent of cue validity, the typically developing children had faster reaction times to visual targets than the children with ADHD [F(1,28) = 4.26, p < .048]; although the effects were in the same direction, for accuracy this main effect did not reach significance for visual discrimination [F(1,28) = 3.76, p > .05]. The overall group effects were similar for the auditory targets: faster overall reaction times [F(1,28) = 5.97, p < .02] and higher accuracy [F(1,28) = 4.88, p < .03]

Discussion

In the present EEG study of attentional control, we found that during a cross-modal attention task, a cue to expect a visual target induced a decrease in posterior alpha EEG activity for the typically developing children but not the children with ADHD. The posterior alpha decrease was correlated with the behavioral benefits imparted by the cues in the typical children but not so in the ADHD children. Moreover, posterior alpha activity was anticorrelated with a frontal theta activity on a

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Previous studies have shown that impaired goal-directed alpha lateralization and functional disconnection within attention networks during the cue period are significant features of attention-deficit/hyperactivity disorder (ADHD). This study aimed to explore the role of brain oscillations in the visual search process, focusing on target-induced posterior alpha lateralization, midfrontal theta synchronization, and their functional connection in children with ADHD.
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Abnormal brain oscillations in children with ADHD indicate insufficient executive control function and the compensation of attention networks for attention deficits in visual selective attention. Cross-frequency disconnection reflects the common deficiency of executive control in the gating of target information. Our findings provide novel evidence for interpreting the features of brain oscillations during stimulus-driven selective attention in children with ADHD.
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In the past two decades, a growing number of studies of ADHD samples have taken advantage of advances in EEG signal processing, called time-frequency analyses, that combine the strengths of QEEG and ERP approaches and provide richer information on sub-second changes of brain activity at different frequencies (available in QEEG, but not ERP studies) and stages of stimulus processing (available in ERP, but not QEEG studies) (Herrmann et al., 2014; Loo et al., 2015; Makeig et al., 2004). Specifically, time-frequency analyses quantify event-related increases in power, also sometime called event-related synchronization (ERS), as well as decreases in power, or event-related desynchronization (ERD), relative to pre-stimulus power (Loo et al., 2015; Mazaheri and Picton, 2005). Mean event-related power changes across trials are often summarized in so-called event-related spectral perturbations (ERSP) (Makeig, 1993; Makeig et al., 2004).
Previous studies have associated attention-deficit/hyperactivity disorder (ADHD) with several alterations in electroencephalographic (EEG) activity. Time-frequency analyses capturing event-related power modulations are becoming an increasingly popular approach, but a systematic synthesis of the time-frequency literature in ADHD is currently lacking. We conducted the first systematic review and meta-analysis of time-frequency studies of children and adults with ADHD in comparison to neurotypical controls. Searches via Medline, Embase, and Web of Science, as well as reference lists, identified 28 eligible articles published until March 2021. Of these, 13 articles with relevant data were included in a multi-level meta-analysis. Most studies examined power modulations of alpha, theta and/or beta frequencies (N = 21/28), and focused on children (N = 17/28). Meta-analyses showed significantly weaker theta increases (Cohen's d = −0.25, p = 0.039; N_ADHD = 346, N_CONTROL = 327), alpha decreases (d = 0.44, p < 0.001; N_ADHD = 564, N_CONTROL = 450), and beta increases (Cohen's d = −0.33, p < 0.001; N_ADHD = 222, N_CONTROL = 263) in individuals with ADHD relative to controls. These patterns indicate broad brain-oscillatory alterations in individuals with ADHD with small (theta) and small-to-moderate (alpha and beta) effect sizes. These group differences were partly consistent when repeating analyses by age group (<18 and 18+ years) and task type (cognitive control, working memory, and simple attention tasks). Overall, our findings identify widespread event-related brain-oscillatory alterations in individuals with ADHD during a range of neurocognitive functions. Future research requires larger samples, a broader range of frequency bands (including delta and gamma) during a wider type of cognitive-affective processes, and should clarify whether atypical event-related power profiles are ADHD-specific or shared with other neuropsychiatric conditions.
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Citation Excerpt :
The non-constrained experimental setting of 5CSRTT, which engages additional behavioral mechanisms, such as head orientation to adjust behavioral performance, may also have contributed to masking the beneficial effect of optogenetic stimulation on task performance. Deficits in error monitoring (Kerns et al., 2005; van Veen and Carter, 2006) and attention network function (Mazaheri et al., 2010; Roiser et al., 2013) are common to many psychiatric disorders, including ADHD, schizophrenia, and autism spectrum disorder. The link between these cognitive deficits and distinct neural circuits remains unclear.
The frontal cortex, especially the anterior cingulate cortex area (ACA), is essential for exerting cognitive control after errors, but the mechanisms that enable modulation of attention to improve performance after errors are poorly understood. Here we demonstrate that during a mouse visual attention task, ACA neurons projecting to the visual cortex (VIS; ACA_VIS neurons) are recruited selectively by recent errors. Optogenetic manipulations of this pathway collectively support the model that rhythmic modulation of ACA_VIS neurons in anticipation of visual stimuli is crucial for adjusting performance following errors. 30-Hz optogenetic stimulation of ACA_VIS neurons in anesthetized mice recapitulates the increased gamma and reduced theta VIS oscillatory changes that are associated with endogenous post-error performance during behavior and subsequently increased visually evoked spiking, a hallmark feature of visual attention. This frontal sensory neural circuit links error monitoring with implementing adjustments of attention to guide behavioral adaptation, pointing to a circuit-based mechanism for promoting cognitive control.

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View full text

Archival ReportFunctional Disconnection of Frontal Cortex and Visual Cortex in Attention-Deficit/Hyperactivity Disorder

Background

Methods

Results

Conclusions

Section snippets

Subjects and Inclusion Criteria

Behavioral Data

Discussion

Trends Cogn Sci

Trends Cogn Sci

Brain Res Rev

Neural Netw

J Am Acad Child Adolesc Psychiatry

Neuroimage.

Neuron

Brain Res Cogn Brain Res

Brain Res Brain Res Rev

Trends Neurosci

Clin Neurophysiol

Biol Psychiatry

Clin Neurophysiol

Dynamic predictions: Oscillations and synchrony in top-down processing

Nat Rev Neurosci

Prestimulus cortical activity is correlated with speed of visuomotor processing

J Cogn Neurosci

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

J Neurosci

Archival Report
Functional Disconnection of Frontal Cortex and Visual Cortex in Attention-Deficit/Hyperactivity Disorder