Aberrant neural activity in the peritumoral cortex underlies the progression of tumor-associated seizures

Bibi L. J. Bouwen, Anne Bolleboom, Yuanhong Tang, Zhaofei Yu, Anna van der Stap, Jort A. van Rij, Vera van Dis, Clemens M. F. Dirven, Chris I. De Zeeuw, Olaf van Tellingen, Jian K. Liu, Arnaud J. P. E. Vincent () and Zhenyu Gao ()
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Bibi L. J. Bouwen: Erasmus Medical Center, Department of Neuroscience
Anne Bolleboom: Erasmus Medical Center, Department of Neuroscience
Yuanhong Tang: Peking University, School of Computer Science, Institute for Artificial Intelligence
Zhaofei Yu: Peking University, School of Computer Science, Institute for Artificial Intelligence
Anna van der Stap: Erasmus Medical Center, Department of Neuroscience
Jort A. van Rij: Erasmus Medical Center, Department of Neuroscience
Vera van Dis: Erasmus Medical Center, Department of Pathology
Clemens M. F. Dirven: Erasmus Medical Center, Department of Neurosurgery
Chris I. De Zeeuw: Erasmus Medical Center, Department of Neuroscience
Olaf van Tellingen: The Netherlands Cancer Institute, Division of Pharmacology
Jian K. Liu: University of Birmingham, School of Computer Science
Arnaud J. P. E. Vincent: Erasmus Medical Center, Department of Neurosurgery
Zhenyu Gao: Erasmus Medical Center, Department of Neuroscience

Nature Communications, 2025, vol. 16, issue 1, 1-19

Abstract: Abstract Seizures are frequent complications in brain tumor patients, yet the underlying neuronal mechanisms remain poorly defined. Here, we examined pathophysiological alterations in the peritumoral cortex of patients undergoing tumor resection. The synaptic activity, dendritic spine density, and gene expression of peritumoral pyramidal neurons differed significantly between patients with and without seizures. Using an inducible glioma rodent model, we characterized the progression of these alterations and their predictive value for seizure initiation. Computational simulations revealed that human cortical neurons are highly susceptible to synaptic and dendritic perturbations, which induce paroxysmal depolarizing shifts (PDS) in affected networks. Longitudinal analyses post-surgery showed that PDS were detectable prior to seizure onset in a subset of patients and reliably predicted post-resection seizure occurrence. These findings elucidate key neuronal substrates of tumor-associated seizures and suggest PDS as a potential biomarker for seizure risk, offering a foundation for targeted diagnostic and therapeutic strategies.

Date: 2025
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DOI: 10.1038/s41467-025-66226-5

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