The neurophysiological effect of mild hypothermia in gyrencephalic brains submitted to ischemic stroke and spreading depolarizations

Front Neurosci. 2024 Mar 14:18:1302767. doi: 10.3389/fnins.2024.1302767. eCollection 2024.

Abstract

Objective: Characterize the neurophysiological effects of mild hypothermia on stroke and spreading depolarizations (SDs) in gyrencephalic brains.

Methods: Left middle cerebral arteries (MCAs) of six hypothermic and six normothermic pigs were permanently occluded (MCAo). Hypothermia began 1 h after MCAo and continued throughout the experiment. ECoG signals from both frontoparietal cortices were recorded. Five-minute ECoG epochs were collected 5 min before, at 5 min, 4, 8, 12, and 16 h after MCAo, and before, during, and after SDs. Power spectra were decomposed into fast (alpha, beta, and gamma) and slow (delta and theta) frequency bands.

Results: In the vascular insulted hemisphere under normothermia, electrodes near the ischemic core exhibited power decay across all frequency bands at 5 min and the 4th hour after MCAo. The same pattern was registered in the two furthest electrodes at the 12th and 16th hour. When mild hypothermia was applied in the vascular insulted hemispheres, the power decay was generalized and seen even in electrodes with uncompromised blood flow. During SD analysis, hypothermia maintained increased delta and beta power during the three phases of SDs in the furthest electrode from the ischemic core, followed by the second furthest and third electrode in the beta band during preSD and postSD segments. However, in hypothermic conditions, the third electrode showed lower delta, theta, and alpha power.

Conclusion: Mild hypothermia attenuates all frequency bands in the vascularly compromised hemisphere, irrespective of the cortical location. During SD formation, it preserves power spectra more significantly in electrodes further from the ischemic core.

Keywords: ECoG recording; mild hypothermia; power spectrum of frequency bands; spreading depolarization; stroke progression.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. ES was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; no. 462569370) and by Consejo Nacional de Humanidades, Ciencias y Tecnologías (National Council of Humanities, Sciences, and Technologies; Reference: CF-2023-G-204). RD-P was supported by a scholarship granted by the Consejo Mexiquense de Ciencia y Tecnología del Estado de México (Council of Science and Technology from the Estate of Mexico; Reference: 2021BPS2-E0405). FR-C was supported by the Consejo Nacional de Ciencia y Tecnología of Mexico (CONACyT, National Council of Science and Technology; Reference: 2019-000021-01 ETF-00514).