Contralesional hippocampal spreading depolarization promotes functional recovery after stroke

Andrew K. J. Boyce (), Yannick Fouad, Renaud C. Gom, Donovan M. Ashby, Cristina Martins-Silva, Leonardo Molina, Tamas Füzesi, Carina Ens, Wilten Nicola, Alexander McGirr, G. Campbell Teskey and Roger J. Thompson ()
Additional contact information
Andrew K. J. Boyce: University of Calgary
Yannick Fouad: University of Calgary
Renaud C. Gom: University of Calgary
Donovan M. Ashby: University of Calgary
Cristina Martins-Silva: Federal University of Espírito Santo
Leonardo Molina: University of Calgary
Tamas Füzesi: University of Calgary
Carina Ens: University of Calgary
Wilten Nicola: University of Calgary
Alexander McGirr: University of Calgary
G. Campbell Teskey: University of Calgary
Roger J. Thompson: University of Calgary

Nature Communications, 2025, vol. 16, issue 1, 1-20

Abstract: Abstract Ischemic stroke, brain tissue infarction following obstructed cerebral blood flow, leads to long-term neurological deficits and death. While neocortex is a commonly affected region with established preclinical models, less is known about deeper brain strokes, despite having unique neurological outcomes. We induced focal ischemic stroke while simultaneously monitoring neuronal activity in awake behaving Thy1-GCaMP6f mice by delivering and collecting light through bilateral fiberoptic implants. Unilateral hippocampal stroke resulted in atypical wandering behavior coincident with ipsilesional terminal spreading depolarization (sustained increase in GCaMP6f fluorescence). Ischemia induced seizures that propagated to the contralesional hippocampus triggering a transient spreading depolarization, predominantly in females. Hippocampal stroke impaired contextual fear conditioning acquired pre-stroke. Yet, 7 days post-stroke, contextual fear conditioning was only improved in mice with contralesional spreading depolarization. Blunting peri-stroke contralesional spreading depolarization prevented recovery of hippocampus-dependent learning. Together, we show that regionally isolated deleterious and beneficial spreading depolarizations can occur concurrently in the murine brain during acute stroke.

Date: 2025
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DOI: 10.1038/s41467-025-57119-8

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