Dynamic modulation of frontal theta power predicts cognitive ability in infancy.
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ABSTRACT:
SUBMITTER: Braithwaite EK
PROVIDER: S-EPMC7393453 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Investigations into the neurophysiological underpinnings of control suggest that frontal theta activity is increased with the need for control. However, these studies typically show this link by reporting associations between increased theta and RT slowing - a process that is contemporaneous with cognitive control but does not strictly reflect the specific use of control. In this study, we assessed frontal theta responses that underpinned the switch cost in task switching - a specific index of cognitive control that does not rely exclusively on RT slowing. Here, we utilised a single-trial regression approach to assess 1) how cognitive control demands beyond simple RT slowing were linked to midfrontal theta and 2) whether midfrontal theta effects remained stable over time. In a large cohort that included a longitudinal subsample, we found that midfrontal theta was modulated by switch costs, with enhanced theta power when preparing to switch vs. repeating a task. These effects were reliable after a two-year interval (Cronbach's α.39-0.74). In contrast, we found that trial-by-trial modulations of midfrontal theta power predicted the size of the switch cost - so that switch trials with increased theta produced smaller switch costs. Interestingly, these relationships between theta and behaviour were less stable over time (Cronbach's α 0-0.61), with participants first using both delta and theta bands to influence behaviour whereas after two years only theta associations with behaviour remained. Together, these findings suggest midfrontal theta supports the need for control beyond simple RT slowing and reveal that midfrontal theta effects remain relatively stable over time.
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Project description:The implications of the substantial individual differences in infant sleep for early brain development remain unclear. Here, we examined whether night sleep quality relates to daytime brain activity, operationalized through measures of EEG theta power and its dynamic modulation, which have been previously linked to later cognitive development. For this longitudinal study, 76 typically developing infants were studied (age: 4-14 months, 166 individual study visits) over the course of 6 months with one, two, three, or four lab visits. Habitual sleep was measured with a 7-day sleep diary and actigraphy, and the Brief Infant Sleep Questionnaire. Twenty-channel EEG was recorded while infants watched multiple rounds of videos of women singing nursery rhymes; oscillatory power in the theta band was extracted. Key metrics were average theta across stimuli and the slope of change in theta within the first novel movie. Both objective and subjective sleep assessment methods showed a relationship between more night waking and higher overall theta power and reduced dynamic modulation of theta over the course of the novel video stimuli. These results may indicate altered learning and consolidation in infants with more disrupted night sleep, which may have implications for cognitive development.
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Project description:Focal electrical stimulation of the brain incites a cascade of neural activity that propagates from the stimulated region to both nearby and remote areas, offering the potential to control the activity of brain networks. Understanding how exogenous electrical signals perturb such networks in humans is key to its clinical translation. To investigate this, we applied electrical stimulation to subregions of the medial temporal lobe in 26 neurosurgical patients fitted with indwelling electrodes. Networks of low-frequency (5-13?Hz) spectral coherence predicted stimulation-evoked increases in theta (5-8?Hz) power, particularly when stimulation was applied in or adjacent to white matter. Stimulation tended to decrease power in the high-frequency broadband (HFB; 50-200?Hz) range, and these modulations were correlated with HFB-based networks in a subset of subjects. Our results demonstrate that functional connectivity is predictive of causal changes in the brain, capturing evoked activity across brain regions and frequency bands.
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Project description:Mid-frontal theta activity underlies cognitive control. These 4-8 Hz rhythms are modulated by cortical dopamine and can be abnormal in patients with Parkinson's disease (PD). Here, we investigated mid-frontal theta deficits in PD patients during a task explicitly involving cognitive control. We collected scalp EEG from high-performing PD patients and demographically matched controls during performance of a modified Simon reaction-time task. This task involves cognitive control to adjudicate response conflict and error-related adjustments. Task performance of PD patients was indistinguishable from controls, but PD patients had less mid-frontal theta modulations around cues and responses. Critically, PD patients had attenuated mid-frontal theta activity specifically associated with response conflict and post-error processing. These signals were unaffected by medication or motor scores. Post-error mid-frontal theta activity was correlated with disease duration. Classification of control vs. PD from these data resulted in a specificity of 69% and a sensitivity of 72%. These findings help define the scope of mid-frontal theta aberrations during cognitive control in PD, and may provide insight into the nature of PD-related cognitive dysfunction.
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Project description:Frontal-midline theta (FMT) oscillations are increased in amplitude during cognitive control tasks. Since these tasks often conflate cognitive control and cognitive effort, it remains unknown if FMT amplitude maps onto cognitive control or effort. To address this gap, we utilized the glucose facilitation effect to manipulate cognitive effort without changing cognitive control demands. We performed a single-blind, crossover human study in which we provided participants with a glucose drink (control session: volume-matched water) to reduce cognitive effort and improve performance on a visuospatial working memory task. Following glucose consumption, participants performed the working memory task at multiple time points of a 3-h window to sample across the rise and fall of blood glucose. Using high-density electroencephalography (EEG), we calculated FMT amplitude during the delay period of the working memory task. Source localization analysis revealed that FMT oscillations originated from bilateral prefrontal cortex. We found that glucose increased working memory accuracy during the high working memory load condition but decreased FMT amplitude. The decrease in FMT amplitude coincided with both peak blood glucose elevation and peak performance enhancement for glucose relative to water. Therefore, the positive association between glucose consumption and task performance provided causal evidence that the amplitude of FMT oscillations may correspond to cognitive effort, rather than cognitive control. Due to the COVID-19 pandemic, data collection was terminated prematurely; the preliminary nature of these findings due to small sample size should be contextualized by rigorous experimental design and use of a novel causal perturbation to dissociate cognitive effort and cognitive control.NEW & NOTEWORTHY We investigated whether frontal-midline theta (FMT) oscillations tracked with cognitive control or cognitive effort by simultaneous manipulation of cognitive control demands in a working memory task and causal perturbation of cognitive effort using glucose consumption. Facilitation of performance from glucose consumption corresponded with decreased FMT amplitude, which provided preliminary causal evidence for a relationship between FMT amplitude with cognitive effort.
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Project description:The subsequent memory paradigm, according to which cerebral activity for later remembered (LR) and later forgotten (LF) items is contrasted, can be used to characterize the processes necessary for successful memory encoding. Previous simultaneous electroencephalography/functional magnetic resonance imaging (EEG/fMRI) memory studies suggest an inverse relationship between frontal theta band power and the blood oxygenation level dependent (BOLD) signal in the default mode network (DMN). The principal aim of this EEG/fMRI study was to test the hypothesis that this putative theta-DMN relationship is less evident in LF compared with LR trials. Fourteen healthy participants performed an episodic memory task in which pictorial stimuli were presented during encoding, and categorized (as LR or LF) by subsequent memory performance. For each encoding trial, the mean of the Hilbert envelope of the theta signal from 400 to 800 ms after stimulus presentation was calculated. To integrate the EEG and fMRI data, general linear models (GLMs) were used to assess the extent to which these single-trial theta values (as modulators of the main effect of stimulus) predicted DMN BOLD signal change, using: (i) whole-head univariate GLMs and (ii) GLMs in which the outcome variable was the time-course of a DMN component derived from spatial independent component analysis of the fMRI data. Theta was significantly greater for LR than LF stimuli. Furthermore, the inverse relationship between theta and BOLD in the DMN was consistently stronger for LR than LF pictures. These findings imply that theta oscillations are key to attenuating processes which may otherwise impair memory encoding.
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Project description:BackgroundDisrupted proactive cognitive control, a form of early selection and active goal maintenance, is hypothesized to underlie the broad cognitive deficits observed in patients with schizophrenia (SPs). Current research suggests that the disrupted activation within and connectivity between regions of the cognitive control network contribute to disrupted proactive cognitive control; however, no study has examined these mechanisms using an AX Continuous Performance Test task in schizophrenia.MethodsTwenty-six SPs (17 male subjects; mean age 34.46 ± 8.77 years) and 28 healthy control participants (HCs; 16 male subjects; mean age 31.43 ± 7.23 years) underwent an electroencephalogram while performing the AX Continuous Performance Test. To examine the extent of activation and level of connectivity within the cognitive control network, power, intertrial phase clustering, and intersite phase clustering metrics were calculated and analyzed.ResultsSPs exhibited expected general decrements in behavioral performance relative to HCs and a more selective deficit in conditions requiring proactive cognitive control. Additionally, SPs exhibited deficits in midline theta power and connectivity during proactive cognitive control trials. Specifically, HCs exhibited significantly greater theta power for B cues relative to A cues, whereas SPs exhibited no significant differences between A- and B-cue theta power. Additionally, differential theta connectivity patterns were observed in SPs and HCs. Behavioral measures of proactive cognitive control predicted functional outcomes in SPs.ConclusionsThis study suggests that low-frequency midline theta activity is selectively disrupted during proactive cognitive control in SPs. The disrupted midline theta activity may reflect a failure of SPs to proactively recruit cognitive control processes.
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Project description:BackgroundCognitive dysfunction is a major feature of Parkinson's disease (PD), but the pathophysiology remains unknown. One potential mechanism is abnormal low-frequency cortical rhythms which engage cognitive functions and are deficient in PD. We tested the hypothesis that mid-frontal delta/theta rhythms predict cognitive dysfunction in PD.MethodWe recruited 100 patients with PD and 49 demographically similar control participants who completed a series of cognitive control tasks, including the Simon, oddball and interval-timing tasks. We focused on cue-evoked delta (1-4 Hz) and theta (4-7 Hz) rhythms from a single mid-frontal EEG electrode (cranial vertex (Cz)) in patients with PD who were either cognitively normal, with mild-cognitive impairments (Parkinson's disease with mild-cognitive impairment) or had dementia (Parkinson's disease dementia).ResultsWe found that PD-related cognitive dysfunction was associated with increased response latencies and decreased mid-frontal delta power across all tasks. Within patients with PD, the first principal component of evoked electroencephalography features from a single electrode (Cz) strongly correlated with clinical metrics such as the Montreal Cognitive Assessment score (r=0.34) and with National Institutes of Health Toolbox Executive Function score (r=0.46).ConclusionsThese data demonstrate that cue-evoked mid-frontal delta/theta rhythms directly relate to cognition in PD. Our results provide insight into the nature of low-frequency frontal rhythms and suggest that PD-related cognitive dysfunction results from decreased delta/theta activity. These findings could facilitate the development of new biomarkers and targeted therapies for cognitive symptoms of PD.
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Project description:There is increasing evidence that the medial prefrontal cortex participates in conflict and feedback monitoring while the subthalamic nucleus adjusts actions. Yet how these two structures coordinate their activity during cognitive control remains poorly understood. We recorded from the human prefrontal cortex and the subthalamic nucleus simultaneously while participants (n = 22) performed a novel task involving high conflict trials, complete response inhibition trials, and trial-to-trial behavioural adaptations to conflict and errors. Overall, we found that within-trial adaptions to both conflict and complete response inhibition involved changes in the theta band while across-trial behavioural adaptations to both conflict and errors involved changes in the beta band (P < 0.05). Yet the role each region's theta and beta oscillations played during the task differed significantly between the two sites. Trials that involved either within-trial conflict or complete response inhibition were associated with increased theta phase synchrony between the medial prefrontal cortex and the subthalamic nucleus (P < 0.05). Despite increased synchrony, however, increases in prefrontal theta power were associated with response inhibition, while increases in subthalamic theta power were associated with response execution (P < 0.05). In the beta band, post-response increases in prefrontal beta power were suppressed when the completed trial contained either conflict or an erroneous response (P < 0.05). Subthalamic beta power, on the other hand, was only modified during the subsequent trial that followed a conflict or error trial. Notably, these adaptation trials exhibited slower response times (P < 0.05), suggesting that both brain regions contribute to across-trial adaptations but do so at different stages of the adaptation process. Taken together, our data shed light on the mechanisms underlying within-trial and across-trial cognitive control and how disruption of this network can negatively impact cognition. More broadly, however, our data also demonstrate that the specific role of a brain region, rather than the frequency being utilized, governs the behavioural correlates of oscillatory activity.
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Project description:ObjectiveAngelman syndrome (AS) is a severe neurodevelopmental disorder caused by loss of function of the maternally inherited UBE3A gene in neurons. Promising disease-modifying treatments to reinstate UBE3A expression are under development and an early measure of treatment response is critical to their deployment in clinical trials. Increased delta power in EEG recordings, reflecting abnormal neuronal synchrony, occurs in AS across species and correlates with genotype. Whether delta power provides a reliable biomarker for clinical symptoms remains unknown.MethodsWe analyzed combined EEG recordings and developmental assessments in a large cohort of individuals with AS (N = 82 subjects, 133 combined EEG and cognitive assessments, 1.08-28.16 years; 32F) and evaluated delta power as a biomarker for cognitive function, as measured by the Bayley Cognitive Score. We examined the robustness of this biomarker to varying states of consciousness, recording techniques and analysis procedures.ResultsDelta power predicted the Bayley Scale cognitive score (P < 10-5 , R2 = 0.9374) after controlling for age (P < 10-24 ), genotype:age (P < 10-11 ), and repeat assessments (P < 10-8 ), with the excellent fit on cross validation (R2 = 0.95). There were no differences in model performance across states of consciousness or bipolar versus average montages (ΔAIC < 2). Models using raw data excluding frontal channels outperformed other models (ΔAIC > 4) and predicted performance in expressive (P = 0.0209) and receptive communication (P < 10-3 ) and fine motor skills (P < 10-4 ).InterpretationDelta power is a simple, direct measure of neuronal activity that reliably correlates with cognitive function in AS. This electrophysiological biomarker offers an objective, clinically relevant endpoint for treatment response in emerging clinical trials.
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