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Alpha desynchronization and fronto-parietal connectivity during spatial working memory encoding deficits in ADHD: A simultaneous EEG-fMRI study.

ABSTRACT: The underlying mechanisms of alpha band (8-12 Hz) neural oscillations are of importance to the functioning of attention control systems as well as to neuropsychiatric conditions that are characterized by deficits of that system, such as attention deficit hyperactivity disorder (ADHD). The objectives of the present study were to test if visual encoding-related alpha event-related desynchronization (ERD) correlates with fronto-parieto-occipital connectivity, and whether this is disrupted in ADHD during spatial working memory (SWM) performance. We acquired EEG concurrently with fMRI in thirty boys (12-16 yrs. old, 15 with ADHD), during SWM encoding. Psychophysiological connectivity analyses indicated that alpha ERD during SWM encoding was associated with both occipital activation and fronto-parieto-occipital functional connectivity, a finding that expands on prior associations between alpha ERD and occipital activation. This finding provides novel support for the interpretation of alpha ERD (and the associated changes in occipital activation) as a phenomenon that involves, and perhaps arises as a result of, top-down network interactions. Alpha ERD was associated less strongly with occipital activity, but associated more strongly with fronto-parieto-occipital connectivity in ADHD, consistent with a compensatory attentional response. Additionally, we illustrate that degradation of EEG data quality by MRI-amplified motion artifacts is robust to existing cleaning algorithms and is significantly correlated with hyperactivity symptoms and the ADHD Combined Type diagnosis. We conclude that persistent motion-related MR artifacts in EEG data can increase variance and introduce bias in interpretation of group differences in populations characterized by hypermobility--a clear limitation of current-state EEG-fMRI methodology.

SUBMITTER: Lenartowicz A

PROVIDER: S-EPMC4761724 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Alpha desynchronization and fronto-parietal connectivity during spatial working memory encoding deficits in ADHD: A simultaneous EEG-fMRI study.

Lenartowicz Agatha A Lu Steven S Rodriguez Cameron C Lau Edward P EP Walshaw Patricia D PD McCracken James T JT Cohen Mark S MS Loo Sandra K SK

NeuroImage. Clinical 20160206

The underlying mechanisms of alpha band (8-12 Hz) neural oscillations are of importance to the functioning of attention control systems as well as to neuropsychiatric conditions that are characterized by deficits of that system, such as attention deficit hyperactivity disorder (ADHD). The objectives of the present study were to test if visual encoding-related alpha event-related desynchronization (ERD) correlates with fronto-parieto-occipital connectivity, and whether this is disrupted in ADHD d ...[more]

PMID: 26955516

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Project description:BackgroundEEG studies of working memory (WM) have demonstrated load dependent frequency band modulations. FMRI studies have localized load modulated activity to the dorsolateral prefrontal cortex (DLPFC), medial prefrontal cortex (MPFC), and posterior parietal cortex (PPC). Recently, an EEG-fMRI study found that low frequency band (theta and alpha) activity negatively correlated with the BOLD signal during the retention phase of a WM task. However, the coupling of higher (beta and gamma) frequencies with the BOLD signal during WM is unknown.MethodologyIn 16 healthy adult subjects, we first investigated EEG-BOLD signal correlations for theta (5-7 Hz), alpha1 (8-10), alpha2 (10-12 Hz), beta1 (13-20), beta2 (20-30 Hz), and gamma (30-40 Hz) during the retention period of a WM task with set size 2 and 5. Secondly, we investigated whether load sensitive brain regions are characterised by effects that relate frequency bands to BOLD signals effects.Principal findingsWe found negative theta-BOLD signal correlations in the MPFC, PPC, and cingulate cortex (ACC and PCC). For alpha1 positive correlations with the BOLD signal were found in ACC, MPFC, and PCC; negative correlations were observed in DLPFC, PPC, and inferior frontal gyrus (IFG). Negative alpha2-BOLD signal correlations were observed in parieto-occipital regions. Beta1-BOLD signal correlations were positive in ACC and negative in precentral and superior temporal gyrus. Beta2 and gamma showed only positive correlations with BOLD, e.g., in DLPFC, MPFC (gamma) and IFG (beta2/gamma). The load analysis revealed that theta and--with one exception--beta and gamma demonstrated exclusively positive load effects, while alpha1 showed only negative effects.ConclusionsWe conclude that the directions of EEG-BOLD signal correlations vary across brain regions and EEG frequency bands. In addition, some brain regions show both load sensitive BOLD and frequency band effects. Our data indicate that lower as well as higher frequency brain oscillations are linked to neurovascular processes during WM.

Project description:Background: Potentially curative epilepsy surgery can be offered if a single, discrete epileptogenic zone (EZ) can be identified. For individuals in whom there is no clear concordance between clinical localization, scalp EEG, and imaging data, intracranial EEG (icEEG) may be needed to confirm a predefined hypothesis regarding irritative zone (IZ), seizure onset zone (SOZ), and EZ prior to surgery. However, icEEG has limited spatial sampling and may fail to reveal the full extent of epileptogenic network if predefined hypothesis is not correct. Simultaneous icEEG-fMRI has been safely acquired in humans and allows exploration of neuronal activity at the whole-brain level related to interictal epileptiform discharges (IED) captured intracranially. Methods: We report icEEG-fMRI in eight patients with refractory focal epilepsy who had resective surgery and good postsurgical outcome. Surgical resection volume in seizure-free patients post-surgically reflects confirmed identification of the EZ. IEDs on icEEG were classified according to their topographic distribution and localization (Focal, Regional, Widespread, and Non-contiguous). We also divided IEDs by their location within the surgical resection volume [primary IZ (IZ1) IED] or outside [secondary IZ (IZ2) IED]. The distribution of fMRI blood oxygen level-dependent (BOLD) changes associated with individual IED classes were assessed over the whole brain using a general linear model. The concordance of resulting BOLD map was evaluated by comparing localization of BOLD clusters with surgical resection volume. Additionally, we compared the concordance of BOLD maps and presence of BOLD clusters in remote brain areas: precuneus, cuneus, cingulate, medial frontal, and thalamus for different IED classes. Results: A total of 38 different topographic IED classes were identified across the 8 patients: Focal (22) and non-focal (16, Regional = 9, Widespread = 2, Non-contiguous = 5). Twenty-nine IEDs originated from IZ1 and 9 from IZ2. All IED classes were associated with BOLD changes. BOLD maps were concordant with the surgical resection volume for 27/38 (71%) IED classes, showing statistical global maximum BOLD cluster or another cluster in the surgical resection volume. The concordance of BOLD maps with surgical resection volume was greater (p < 0.05) for non-focal (87.5%, 14/16) as compared to Focal (59%, 13/22) IED classes. Additionally, BOLD clusters in remote cortical and deep brain areas were present in 84% (32/38) of BOLD maps, more commonly (15/16; 93%) for non-focal IED-related BOLD maps. Conclusions: Simultaneous icEEG-fMRI can reveal BOLD changes at the whole-brain level for a wide range of IEDs on icEEG. BOLD clusters within surgical resection volume and remote brain areas were more commonly seen for non-focal IED classes, suggesting that a wider hemodynamic network is at play.

Project description:BackgroundAttention-Deficit/Hyperactivity Disorder (ADHD) is a prevalent, complex disorder which is characterized by symptoms of inattention, hyperactivity, and impulsivity. Convergent evidence from neurobiological studies of ADHD identifies dysfunction in fronto-striatal-cerebellar circuitry as the source of behavioural deficits. Recent studies have shown that regions governing basic sensory processing, such as the somatosensory cortex, show abnormalities in those with ADHD suggesting that these processes may also be compromised.MethodsWe used event-related magnetoencephalography (MEG) to examine patterns of cortical rhythms in the primary (SI) and secondary (SII) somatosensory cortices in response to median nerve stimulation, in 9 adults with ADHD and 10 healthy controls. Stimuli were brief (0.2 ms) non-painful electrical pulses presented to the median nerve in two counterbalanced conditions: unpredictable and predictable stimulus presentation. We measured changes in strength, synchronicity, and frequency of cortical rhythms.ResultsHealthy comparison group showed strong event-related desynchrony and synchrony in SI and SII. By contrast, those with ADHD showed significantly weaker event-related desynchrony and event-related synchrony in the alpha (8-12 Hz) and beta (15-30 Hz) bands, respectively. This was most striking during random presentation of median nerve stimulation. Adults with ADHD showed significantly shorter duration of beta rebound in both SI and SII except for when the onset of the stimulus event could be predicted. In this case, the rhythmicity of SI (but not SII) in the ADHD group did not differ from that of controls.ConclusionOur findings suggest that somatosensory processing is altered in individuals with ADHD. MEG constitutes a promising approach to profiling patterns of neural activity during the processing of sensory input (e.g., detection of a tactile stimulus, stimulus predictability) and facilitating our understanding of how basic sensory processing may underlie and/or be influenced by more complex neural networks involved in higher order processing.

Project description:Rising life expectancies coupled with an increasing awareness of age-related cognitive decline have led to the unwarranted use of psychopharmaceuticals, including acetylcholinesterase inhibitors (AChEIs), by significant numbers of healthy older individuals. This trend has developed despite very limited data regarding the effectiveness of such drugs on non-clinical groups and recent work indicates that AChEIs can have negative cognitive effects in healthy populations. For the first time, we use a combination of EEG and simultaneous EEG/fMRI to examine the effects of a commonly prescribed AChEI (donepezil) on cognition in healthy older participants. The short- and long-term impact of donepezil was assessed using two double-blind, placebo-controlled trials. In both cases, we utilised cognitive (paired associates learning (CPAL)) and electrophysiological measures (resting EEG power) that have demonstrated high-sensitivity to age-related cognitive decline. Experiment 1 tested the effects of 5 mg/per day dosage on cognitive and EEG markers at 6-hour, 2-week and 4-week follow-ups. In experiment 2, the same markers were further scrutinised using simultaneous EEG/fMRI after a single 5 mg dose. Experiment 1 found significant negative effects of donepezil on CPAL and resting Alpha and Beta band power. Experiment 2 replicated these results and found additional drug-related increases in the Delta band. EEG/fMRI analyses revealed that these oscillatory differences were associated with activity differences in the left hippocampus (Delta), right frontal-parietal network (Alpha), and default-mode network (Beta). We demonstrate the utility of simple cognitive and EEG measures in evaluating drug responses after acute and chronic donepezil administration. The presentation of previously established markers of age-related cognitive decline indicates that AChEIs can impair cognitive function in healthy older individuals. To our knowledge this is the first study to identify the precise neuroanatomical origins of EEG drug markers using simultaneous EEG/fMRI. The results of this study may be useful for evaluating novel drugs for cognitive enhancement.

Dataset Information

Alpha desynchronization and fronto-parietal connectivity during spatial working memory encoding deficits in ADHD: A simultaneous EEG-fMRI study.

Publications

Alpha desynchronization and fronto-parietal connectivity during spatial working memory encoding deficits in ADHD: A simultaneous EEG-fMRI study.

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