TY - JOUR
T1 - Aberrant neural activity in the peritumoral cortex underlies the progression of tumor-associated seizures
AU - Bouwen, Bibi L. J.
AU - Bolleboom, Anne
AU - Tang, Yuanhong
AU - Yu, Zhaofei
AU - van der Stap, Anna
AU - van Rij, Jort A.
AU - van Dis, Vera
AU - Dirven, Clemens M. F.
AU - De Zeeuw, Chris I.
AU - van Tellingen, Olaf
AU - Liu, Jian K.
AU - Vincent, Arnaud J. P. E.
AU - Gao, Zhenyu
PY - 2025/12/2
Y1 - 2025/12/2
N2 - 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.
AB - 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.
U2 - 10.1038/s41467-025-66226-5
DO - 10.1038/s41467-025-66226-5
M3 - Article
SN - 2041-1723
VL - 16
JO - Nature Communications
JF - Nature Communications
M1 - 10846
ER -