Publication Date

5-27-2024

Journal

Nature Communications

DOI

10.1038/s41467-024-48757-5

PMID

38802334

PMCID

PMC11130179

PubMedCentral® Posted Date

5-27-2024

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

Glioblastoma, Animals, Brain Neoplasms, Mice, Humans, Nerve Net, Glutamic Acid, Neurons, Cerebral Cortex, Calcium Signaling, Disease Models, Animal, Male, Calcium, Female, Cancer in the nervous system, CNS cancer, Astrocyte, Cancer microenvironment, CNS cancer

Abstract

The emergence of glioblastoma in cortical tissue initiates early and persistent neural hyperexcitability with signs ranging from mild cognitive impairment to convulsive seizures. The influence of peritumoral synaptic density, expansion dynamics, and spatial contours of excess glutamate upon higher order neuronal network modularity is unknown. We combined cellular and widefield imaging of calcium and glutamate fluorescent reporters in two glioblastoma mouse models with distinct synaptic microenvironments and infiltration profiles. Functional metrics of neural ensembles are dysregulated during tumor invasion depending on the stage of malignant progression and tumor cell proximity. Neural activity is differentially modulated during periods of accelerated and inhibited tumor expansion. Abnormal glutamate accumulation precedes and outpaces the spatial extent of baseline neuronal calcium signaling, indicating these processes are uncoupled in tumor cortex. Distinctive excitability homeostasis patterns and functional connectivity of local and remote neuronal populations support the promise of precision genetic diagnosis and management of this devastating brain disease.

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