Abstract
Spreading depolarizations (SDs) are a marker of brain injury and have a causative effect on ischemic lesion progression. The hemodynamic responses elicited by SDs are contingent upon the metabolic integrity of the affected tissue, with vasoconstrictive reactions leading to pronounced hypoxia often indicating poor outcomes. The stratification of hemodynamic responses within different cortical layers remains poorly characterized. This pilot study sought to elucidate the depth-specific hemodynamic changes in response to SDs within the gray matter of the gyrencephalic swine brain. Employing a potassium chloride–induced SD model, we utilized multispectral photoacoustic imaging (PAI) to estimate regional cerebral oxygen saturation (rcSO2%) changes consequent to potassium chloride–induced SDs. Regions of interest were demarcated at three cortical depths covering up to 4 mm. Electrocorticography (ECoG) strips were placed to validate the presence of SDs. Through PAI, we detected 12 distinct rcSO2% responses, which corresponded with SDs detected in ECoG. Notably, a higher frequency of hypoxic responses was observed in the deeper cortical layers compared to superficial layers, where hyperoxic and mixed responses predominated (p < 0.001). This data provides novel insights into the differential oxygenation patterns across cortical layers in response to SDs, underlining the complexity of cerebral hemodynamics post-injury.
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No datasets were generated or analysed during the current study.
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Acknowledgements
We thank Alexander Seitel (German Cancer Research Center) for their useful suggestions.
Funding
ES was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation; no. 462569370) and by the National Council of Humanities, Sciences, and Technologies of Mexico (CONAHCyT); reference: CF-2023-G-204. JML-N and MAS-G were supported by the National Council of Humanities, Science, Technology, and Innovation of Mexico (CONAHCyT); reference: 2021–000021-01EXTF-00042 and 2021–000021-01EXTF-00049, respectively.
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ES and RS-P conceived the study and played pivotal roles in designing the research and experimental protocols and wrote the manuscript. JML-N and MAS-G analyzed data and co-wrote the manuscript. NH and TK implemented the PAI system, designed and performed experiments, processed PAI data, and edited the manuscript. PA-P designed the figures. AH-A performed experiments and analyzed data. JAL-A advised on the histological morphology of the pig cerebral cortex. FV, JW, and LM-H provided intellectual and scientific support and revised the manuscript. All authors contributed to the article and approved the submitted version.
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Santos, E., Lopez-Navarro, J.M., Suarez-Gutierrez, M.A. et al. Depth-Specific Hypoxic Responses to Spreading Depolarizations in Gyrencephalic Swine Cortex Unveiled by Photoacoustic Imaging. Transl. Stroke Res. (2024). https://doi.org/10.1007/s12975-024-01247-8
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DOI: https://doi.org/10.1007/s12975-024-01247-8