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Neuronal morphology and physiology, functional brain networks and memory in temporal lobe epilepsy

Linda Douw, Ida A. Nissen, Sophie M.D.D. Fitzsimmons, Fernando A.N. Santos, Arjan Hillebrand, Elisabeth C.W. van Straaten, Cornelis J. Stam, Philip C. De Witt Hamer, Johannes C. Baayen, Martin Klein, Jaap C. Reijneveld, Djai B. Heyer, Matthijs B. Verhoog, René Wilbers, Sarah Hunt, Huibert D. Mansvelder, Jeroen J.G. Geurts, Christiaan P.J. de Kock, Natalia A. Goriounova
doi: https://doi.org/10.1101/2021.01.31.428369
Linda Douw
1Department of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
2Department of Radiology, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, USA
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  • For correspondence: l.douw@vumc.nl
Ida A. Nissen
3Department of Clinical Neurophysiology and MEG Center, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Sophie M.D.D. Fitzsimmons
1Department of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Fernando A.N. Santos
1Department of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Arjan Hillebrand
3Department of Clinical Neurophysiology and MEG Center, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Elisabeth C.W. van Straaten
3Department of Clinical Neurophysiology and MEG Center, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Cornelis J. Stam
3Department of Clinical Neurophysiology and MEG Center, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Philip C. De Witt Hamer
4Department of Neurosurgery, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, VUmc Cancer Center Amsterdam Brain Tumor Center Amsterdam, the Netherlands
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Johannes C. Baayen
4Department of Neurosurgery, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, VUmc Cancer Center Amsterdam Brain Tumor Center Amsterdam, the Netherlands
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Martin Klein
5Department of Medical Psychology, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, VUmc Cancer Center Amsterdam Brain Tumor Center Amsterdam, the Netherlands
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Jaap C. Reijneveld
6Department of Neurology, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, VUmc Cancer Center Amsterdam Brain Tumor Center Amsterdam, the Netherlands
7Stichting Epilepsie Instellingen Nederland (SEIN), Heemstede, the Netherlands
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Djai B. Heyer
8Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Matthijs B. Verhoog
8Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
9Department of Human Biology, Division of Cell Biology, Neuroscience Institute, University of Cape Town, South Africa
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René Wilbers
8Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Sarah Hunt
8Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Huibert D. Mansvelder
8Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Jeroen J.G. Geurts
1Department of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Christiaan P.J. de Kock
8Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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Natalia A. Goriounova
8Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Vrije Universiteit Amsterdam, Amsterdam Neuroscience, the Netherlands
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ABSTRACT

Temporal lobe epilepsy patients are heterogeneous regarding cognitive functioning, with predominant risk of memory deficits. Despite major advances within cellular neuroscience, neuroimaging, and neuropsychology, it remains challenging to integrate memory performance with cellular characteristics and brain network topology. In a unique dataset, we investigate these cross-scale individual differences. Preoperatively, drug-resistant temporal lobe epilepsy patients (n = 31, 15 females) underwent functional magnetic resonance imaging, magnetoencephalography and/or memory testing. Macro-scale network centrality was determined, since the number of integrative functional connections a region has is crucial for memory functioning. Subsequently, non-pathological cortical tissue resected from the lateral middle temporal gyrus (default mode network) was used for single cell morphological (total dendritic length) and electrophysiological patch-clamp analysis (action potential rise speed). We expected greater macro-scale centrality to relate to longer micro-scale dendritic length and faster action potentials, and greater centrality to relate to better memory performance. Greater macro-scale centrality correlated with longer dendritic length and faster action potentials (canonical correlation coefficient = 0.329, p < 0.001). Moreover, greater macro-scale centrality was related to better memory performance (canonical correlation coefficient = 0.234, p = 0.013). We conclude that more complex neuronal morphology and faster action potential kinetics are mirrored by more integrative functional network topology of the middle temporal gyrus, which in turn is associated with better memory functioning. Thus, our cross-scale analyses reveal a significant relationship between cellular and imaging measures of network topology in the brain, which support cognitive performance in these patients.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Link to github added, funding and acknowledgements added, author list corrected.

  • https://github.com/multinetlab-amsterdam/projects/tree/master/multiscale_integration

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Neuronal morphology and physiology, functional brain networks and memory in temporal lobe epilepsy
Linda Douw, Ida A. Nissen, Sophie M.D.D. Fitzsimmons, Fernando A.N. Santos, Arjan Hillebrand, Elisabeth C.W. van Straaten, Cornelis J. Stam, Philip C. De Witt Hamer, Johannes C. Baayen, Martin Klein, Jaap C. Reijneveld, Djai B. Heyer, Matthijs B. Verhoog, René Wilbers, Sarah Hunt, Huibert D. Mansvelder, Jeroen J.G. Geurts, Christiaan P.J. de Kock, Natalia A. Goriounova
bioRxiv 2021.01.31.428369; doi: https://doi.org/10.1101/2021.01.31.428369
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Neuronal morphology and physiology, functional brain networks and memory in temporal lobe epilepsy
Linda Douw, Ida A. Nissen, Sophie M.D.D. Fitzsimmons, Fernando A.N. Santos, Arjan Hillebrand, Elisabeth C.W. van Straaten, Cornelis J. Stam, Philip C. De Witt Hamer, Johannes C. Baayen, Martin Klein, Jaap C. Reijneveld, Djai B. Heyer, Matthijs B. Verhoog, René Wilbers, Sarah Hunt, Huibert D. Mansvelder, Jeroen J.G. Geurts, Christiaan P.J. de Kock, Natalia A. Goriounova
bioRxiv 2021.01.31.428369; doi: https://doi.org/10.1101/2021.01.31.428369

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