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Balancing excitation and inhibition: The role of neural network dynamics in working memory gating

MPS-Authors
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Herzog,  Nadine       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
International Max Planck Research School on Neuroscience of Communication: Function, Structure, and Plasticity, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Cesnaite,  Elena       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Institute for Psychology, Münster University, Germany;

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Steinfath,  Tim Paul       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
International Max Planck Research School on Neuroscience of Communication: Function, Structure, and Plasticity, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Kapralov,  Nikolai       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
International Max Planck Research School on Neuroscience of Communication: Function, Structure, and Plasticity, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Nikulin,  Vadim V.       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Villringer,  Arno       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;

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Janssen,  Lieneke       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Institute of Psychology, Otto von Guericke University Magdeburg, Germany;

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Horstmann,  Annette       
Department Neurology, MPI for Human Cognitive and Brain Sciences, Max Planck Society;
Department of Psychology, Faculty of Medicine, University of Helsinki, Finland;
Integrated Research and Treatment Center Adiposity Diseases, University of Leipzig, Germany;

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Fulltext (public)

Herzog_Cesnaite_2024.pdf
(Publisher version), 19MB

Supplementary Material (public)

Herzog_Cesnaite_2024_Suppl.pdf
(Supplementary material), 691KB

Citation

Herzog, N., Cesnaite, E., Steinfath, T. P., Kapralov, N., Fallon, S. J., Nikulin, V. V., et al. (2024). Balancing excitation and inhibition: The role of neural network dynamics in working memory gating. Imaging Neuroscience, 2: imag-2-00380. doi:10.1162/imag_a_00380/125236.


Cite as: https://hdl.handle.net/21.11116/0000-0011-7AC9-2
Abstract
In the complex landscape of daily life, we continuously balance between maintaining focus despite distractions and flexibly updating focus when needed—a cognitive process governed by a mechanism known as working memory gating. While much research has focused on the neural locus of this mechanism, less is known about the underlying neural dynamics. Here we probe the role of network excitation/inhibition (E/I) dynamics in working memory gating. Utilizing resting-state electroencephalography, we extract two markers of network E/I dynamics: resting-state long-range temporal correlations (LRTCs)—indicative of “critically” balanced E/I dynamics, and the slope of the power spectral density (PSD)—indicative of E/I ratio, and relate them to performance on a working memory gating task, specifically probing distractor-resistant maintenance and flexible updating. Based on previous studies linking stronger LRTCs to enhanced adaptive cognition, we initially expected to observe a similar relation. We find the opposite pattern, however: stronger LRTCs (indicating a more “critical” E/I balance) predicted poorer performance in maintenance-related working memory processes. This challenges the assumption that “near-critical” system dynamics are generally beneficial for cognitive function. Additionally, a flatter PSD slope (indicating a higher E/I ratio) was associated with better maintenance-related performance, particularly in individuals with higher levels of blood phenylalanine and tyrosine (indicating greater central dopamine availability). Notably, both network measures affected performance in all but the updating condition, suggesting a nuanced role of cortical E/I dynamics in overarching maintenance-related working memory processes, distinct from the gating mechanism as such. Our results highlight the complex interplay of network dynamics and neurochemical environments in cognitive function, suggesting implications for targeted interventions in cognitive disorders.