Dataset Information

A simultaneous EEG-fMRI study of thalamic load-dependent working memory delay period activity.

ABSTRACT:

Introduction

Working memory (WM) is an essential component of executive functions which depend on maintaining task-related information online for brief periods in both the presence and absence of interfering stimuli. Active maintenance occurs during the WM delay period, the time between stimulus encoding and subsequent retrieval. Previous studies have extensively documented prefrontal and posterior parietal cortex activity during the WM delay period, but the role of subcortical structures including the thalamus remains to be fully elucidated, especially in humans.

Methods

Using a simultaneous electroencephalogram (EEG)-functional magnetic resonance imaging (fMRI) approach, we investigated the role of the thalamus during the WM delay period in a modified Sternberg paradigm following low and high memory load encoding of naturalistic scenes. During the delay, participants passively viewed scrambled scenes containing similar color and spatial frequency to serve as a perceptual baseline. Individual source estimation was weighted by the location of the thalamic fMRI signal relative to the WM delay period onset.

Results

The effects memory load on maintenance were observed bilaterally in thalamus with higher EEG source amplitudes in the low compared to high load condition occurring 160-390 ms after the onset of the delay period.

Conclusion

The main finding that thalamic activation was elevated during the low compared to high condition despite similar duration of perceptual input and upcoming motor requirements suggests a capacity-limited role for sensory filtering of the thalamus during consolidation of stimuli into WM, where the highest activity occurs when fewer stimuli need to be maintained in the presence of interfering perceptual stimuli during the delay. The results are discussed in the context of theories regarding the role of the thalamus in sensory gating during working memory.

SUBMITTER: Gomes BA

PROVIDER: S-EPMC9997713 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Publications

A simultaneous EEG-fMRI study of thalamic load-dependent working memory delay period activity.

Gomes Bernard A BA Plaska Chelsea Reichert CR Ortega Jefferson J Ellmore Timothy M TM

Frontiers in behavioral neuroscience 20230223

<h4>Introduction</h4>Working memory (WM) is an essential component of executive functions which depend on maintaining task-related information online for brief periods in both the presence and absence of interfering stimuli. Active maintenance occurs during the WM delay period, the time between stimulus encoding and subsequent retrieval. Previous studies have extensively documented prefrontal and posterior parietal cortex activity during the WM delay period, but the role of subcortical structure ...[more]

PMID: 36910125

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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: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.

Project description:IntroductionElectroencephalographic (EEG) data quality is severely compromised when recorded inside the magnetic resonance (MR) environment. Here we characterized the impact of the ballistocardiographic (BCG) artifact on resting-state EEG spectral properties and compared the effectiveness of seven common BCG correction methods to preserve EEG spectral features. We also assessed if these methods retained posterior alpha power reactivity to an eyes closure-opening (EC-EO) task and compared the results from EEG-informed fMRI analysis using different BCG correction approaches.MethodElectroencephalographic data from 20 healthy young adults were recorded outside the MR environment and during simultaneous fMRI acquisition. The gradient artifact was effectively removed from EEG-fMRI acquisitions using Average Artifact Subtraction (AAS). The BCG artifact was corrected with seven methods: AAS, Optimal Basis Set (OBS), Independent Component Analysis (ICA), OBS followed by ICA, AAS followed by ICA, PROJIC-AAS and PROJIC-OBS. EEG signal preservation was assessed by comparing the spectral power of traditional frequency bands from the corrected rs-EEG-fMRI data with the data recorded outside the scanner. We then assessed the preservation of posterior alpha functional reactivity by computing the ratio between the EC and EO conditions during the EC-EO task. EEG-informed fMRI analysis of the EC-EO task was performed using alpha power-derived BOLD signal predictors obtained from the EEG signals corrected with different methods.ResultsThe BCG artifact caused significant distortions (increased absolute power, altered relative power) across all frequency bands. Artifact residuals/signal losses were present after applying all correction methods. The EEG reactivity to the EC-EO task was better preserved with ICA-based correction approaches, particularly when using ICA feature extraction to isolate alpha power fluctuations, which allowed to accurately predict hemodynamic signal fluctuations during the EEG-informed fMRI analysis.DiscussionCurrent software solutions for the BCG artifact problem offer limited efficiency to preserve the EEG spectral power properties using this particular EEG setup. The state-of-the-art approaches tested here can be further refined and should be combined with hardware implementations to better preserve EEG signal properties during simultaneous EEG-fMRI. Existing and novel BCG artifact correction methods should be validated by evaluating signal preservation of both ERPs and spontaneous EEG spectral power.

Dataset Information

A simultaneous EEG-fMRI study of thalamic load-dependent working memory delay period activity.

Introduction

Methods

Results

Conclusion

Publications

A simultaneous EEG-fMRI study of thalamic load-dependent working memory delay period activity.

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