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Stimulus-related modulation in the 1/f slope suggests an impaired inhibition in people with multiple

Poster No:

1654 

Submission Type:

Abstract Submission 

Authors:

Fahimeh Akbarian1,2, Chiara Rossi1,2, Lars Costers3, Marie D'hooghe4, Miguel D'Haeseleer4,5, Guy Nagels2,5,6, Jeroen Van Schependom1,2

Institutions:

1Department of Electronics and Informatics (ETRO), Vrije Universiteit Brussel, Brussels, Belgium, 2AIMS lab, Vrije Universiteit Brussel, Center for Neurosciences, Brussels, Belgium, 3icometrix, Brussels, Belgium, 4National MS Center Melsbroek, Melsbroek, Belgium, 5UZ Brussel, Department of Neurology, Brussels, Belgium, 6St Edmund Hall, University of Oxford, Oxford, UK

First Author:

Fahimeh Akbarian  
Department of Electronics and Informatics (ETRO), Vrije Universiteit Brussel|AIMS lab, Vrije Universiteit Brussel, Center for Neurosciences
Brussels, Belgium|Brussels, Belgium

Co-Author(s):

Chiara Rossi  
Department of Electronics and Informatics (ETRO), Vrije Universiteit Brussel|AIMS lab, Vrije Universiteit Brussel, Center for Neurosciences
Brussels, Belgium|Brussels, Belgium
Lars Costers  
icometrix
Brussels, Belgium
Marie D'hooghe  
National MS Center Melsbroek
Melsbroek, Belgium
Miguel D'Haeseleer  
National MS Center Melsbroek|UZ Brussel, Department of Neurology
Melsbroek, Belgium|Brussels, Belgium
Guy Nagels  
AIMS lab, Vrije Universiteit Brussel, Center for Neurosciences|UZ Brussel, Department of Neurology|St Edmund Hall, University of Oxford
Brussels, Belgium|Brussels, Belgium|Oxford, UK
Jeroen Van Schependom  
Department of Electronics and Informatics (ETRO), Vrije Universiteit Brussel|AIMS lab, Vrije Universiteit Brussel, Center for Neurosciences
Brussels, Belgium|Brussels, Belgium

Introduction:

Multiple sclerosis (MS), an inflammatory and neurodegenerative disease characterized by inhibitory and excitatory synaptic loss (1), imposes a cognitive burden on people with MS (pwMS) with a significant effect on information processing speed and working memory (WM). It has been computationally demonstrated that the balance between excitation and inhibition (E/I) is essential for efficient information processing and WM maintenance. The non-oscillatory or 1/f-like component of the power spectrum of neuronal activity has been hypothesized to provide an accessible marker of E/I balance. The steepness of this 1/f power-law component (denoted as "x" in (1/f)∧x), has been associated with the E/I ratio (2), where a steeper slope indicates a higher level of inhibition (2–4). Gyurkovics et al (5) were the first to report an immediate and possibly transient increase in 1/f slope following an oddball auditory stimulation. In this study, we examine the 1/f slope during a visual-verbal n-back task. We hypothesize that the 1/f slope will be steeper post vs. pre-stimulus during the n-back task, similar to what has been observed in recent studies (5,6). In addition, we hypothesize that an impaired E/I balance – as suggested in pwMS1 - will lead to reduced inhibition during distractor trials. Finally, we will explore to which extent the level of 1/f modulation can be associated with offline cognitive performance.

Methods:

MEG data were recorded from 38 HCs, 19 pwMS treated (pwMS(BZDp)) and 60 pwMS not treated (pwMS(BZDn)) with benzodiazepines, during a visual-verbal n-back task (7) which included 240 target and distractor stimuli with three level of WM loads (0, 1 and 2-back). Data were preprocessed using the OSL library and source reconstructed using an LCMV beamformer (8) and then parceled into 42 parcels. We computed and compared the steepness of the 1/f spectral slope through the FOOOF algorithm (9) in the time windows [-1 0] and [0 1] second peristimulus time for both target and distractor stimulus, for each brain parcel, and different working memory loads. To estimate the periodic alpha power, we corrected the power spectrum density for the fitted aperiodic component. After subtraction of the 1/f component, the periodic alpha power was defined as the average alpha power in the [8-12] Hz band.

Results:

Besides the expected alpha suppression, we observed a steeper 1/f slope after both target and distractor trials suggesting an increase in inhibition following stimulus onset. Importantly, while we observed that higher alpha power is associated with a steeper 1/f slope, the changes of alpha power and 1/f slope after stimulus onset occurred in opposite directions. In line with our hypothesis, pwMS(BZDn) had a flatter 1/f slope after distractor stimuli compared to HCs (p0-back= 0.043, p1-back = 0.02, p2-back = 0.042). We observed a significant positive Pearson correlation between 1/f slope and reaction time, particularly pronounced in the 2-back condition. Our findings corroborate a recent computational study (10) which demonstrated that a higher E/I ratio is associated with a longer reaction time. We also observed a significant Pearson correlation between 1/f slope modulation and visuospatial working memory performance measured by the Brief Visuospatial Memory Test (Revised; BVMT-R). In HCs, a weaker 1/f slope modulation during a WM task correlated with increased spatial working memory, whereas the opposite effect was observed in pwMS.
Supporting Image: Figure1.JPG
Supporting Image: Figure2.JPG
 

Conclusions:

Our findings are consistent with an increase in inhibition following stimulus onset. In pwMS(BZDn), this increase is reduced after distractor stimuli compared to healthy controls, suggesting a less pronounced inhibition of irrelevant information in pwMS in all three conditions. The association of 1/f slope modulation with behavioral and visuospatial WM performance, underscoring the potential significance of the 1/f spectral slope as a valuable marker for task analysis in clinical applications.

Higher Cognitive Functions:

Executive Function, Cognitive Control and Decision Making

Learning and Memory:

Working Memory 2

Modeling and Analysis Methods:

EEG/MEG Modeling and Analysis 1

Novel Imaging Acquisition Methods:

MEG

Keywords:

Cognition
MEG
Other - Working memory; Multiple sclerosis; 1/f slope; Aperiodic activity; N-back task

1|2Indicates the priority used for review

Provide references using author date format

1. Huiskamp, M. et al. (2022), 'Inhibitory synaptic loss drives network changes in multiple sclerosis: An ex vivo to in silico translational study', Multiple Sclerosis Journal 28, 2010–2019.
2. Gao, R. et al. (2017), 'Inferring synaptic excitation/inhibition balance from field potentials', `NeuroImage 158, 70–78.
3. Chini, M. et al. (2022), 'An increase of inhibition drives the developmental decorrelation of neural activity', eLife 11.
4. Akbarian, F. et al. (2023), 'The spectral slope as a marker of excitation/inhibition ratio and cognitive functioning in multiple sclerosis', Human Brain Mapping, 44(17), 5784–5794
5. Gyurkovics, M. et al. (2022), 'Stimulus-Induced Changes in 1/ f -like Background Activity in EEG', The Journal of Neuroscience 42, 7144–7151.
6. Virtue-Griffiths, S. et al. (2022), 'Task-related changes in aperiodic activity are related to visual working memory capacity independent of event-related potentials and alpha oscillations', bioRxiv 2022.01.18.476852. doi:10.1101/2022.01.18.476852.
7. Costers, L. et al. (2020), 'Spatiotemporal and spectral dynamics of multi-item working memory as revealed by the n-back task using MEG', Human Brain Mapping 41, 2431–2446.
8. Woolrich, M. et al. (2011), 'MEG beamforming using Bayesian PCA for adaptive data covariance matrix regularization', NeuroImage 57, 1466–1479.
9. Donoghue, T. et al. (2020), 'Parameterizing neural power spectra into periodic and aperiodic components'. Nature Neuroscience 23, 1655–1665.
10. Calvin, O. L. & Redish, A. D. (2021), 'Global disruption in excitation-inhibition balance can cause localized network dysfunction and Schizophrenia-like context-integration deficits', PLOS Computational Biology 17, e1008985.