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Spreading Diffusion-Restriction Events in the Gyrencephalic Brain After Subarachnoid Hemorrhage Revealed by Continuous Magnetic Resonance Imaging

  • Spreading cortical depolarization
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Abstract

Background

How widely spreading depolarizations (SDs) propagate through the gyrencephalic brain, including sulci and deeper cortical areas, remains an important clinical question. Here, we investigated SDs that occur spontaneously after subarachnoid placement of autologous blood clots in sulci of the juvenile swine brain.

Methods

To investigate the three-dimensional spread of waves, animals underwent continuous diffusion-weighted magnetic resonance imaging (DW-MRI) for up to 6 h following clot placement. SD is the mechanism of the cytotoxic edema of developing infarction that is diagnosed by DW-MRI, and DW-MRI also captures transient diffusion restriction caused by SD in less injured or healthy brains. Here, images (b = 0, 375, and 750) were acquired across five coronal slices with 1.25 × 1.25-mm in-plane resolution and 5-mm slice thickness, and the protocol was repeated every 6.83–9.15 s. Spatial drift correction, temporal smoothing, and signal intensity normalization were applied to generate videos of diffusion signal intensity changes for each coronal slice.

Results

Review of video data from five animals revealed ten discrete events consisting of focal diffusion restriction that propagated through cerebral cortex. All events originated in the cortex surrounding the sulcal clot, either in the gyrus (n = 4) or in the sulcal depth (n = 6). In six cases, two to three independent waves spread simultaneously in medial, lateral, and antero–posterior directions. Waves traveled within sulcal walls, traversed the depths of sulci to re-emerge on the adjacent gyrus, and, in three cases, spread fully around the dorsolateral convexity. One event spread deep to olfactory regions along midline cortex, and no events were observed contralateral to the subarachnoid clot.

Conclusions

Together, these results suggest that SDs in the injured gyrencephalic brain originate near the injury focus and can spread extensively through the cortex to wide and deep uninjured regions. These findings have implications for transient neurologic deficits in the neurocritically ill patient and relevance to patient monitoring and therapeutics.

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Funding

This work was supported by the American Association of Neurological Surgeons/Congress of Neurological Surgeons (AANS/CNS) Joint Section on Cerebrovascular Surgery Robert J. Dempsey, MD, Cerebrovascular Research Award (to CPC) and the Mayfield Education and Research Foundation (to JAH, CPC).

Author information

Authors and Affiliations

  1. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH, USA

    Jed A. Hartings

  2. Department of Brain and Spinal Surgery, Naval Medical Center Portsmouth, Portsmouth, VA, USA

    Christopher P. Carroll

  3. Department of Surgery, Uniformed Services University, Bethesda, MD, USA

    Christopher P. Carroll

  4. Department of Radiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Gregory Lee

Authors
  1. Jed A. Hartings
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  2. Christopher P. Carroll
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  3. Gregory Lee
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Contributions

JAH conceived the study, contributed to experimental design and execution, drafted the manuscript, and approval the final manuscript version. CPC contributed to experimental design, performed surgeries, collected data, edited the manuscript, and approved the final manuscript version. GL designed and executed the magnetic resonance imaging protocols, processed the data, analyzed results, contributed to manuscript preparation, and approved the final manuscript version.

Corresponding author

Correspondence to Jed A. Hartings.

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Copyright Statement

Christopher P. Carroll, LCDR, MC, USN, is a military service member. This work was prepared as part of their official duties. Title 17 U.S.C. 105 provides that "Copyright protection under this title is not available for any work of the United States Government." Title 17 U.S.C. 101 defines a United States Government work as a work prepared by a military service member or employee of the United States Government as part of that person’s official duties.

Disclaimer

The views expressed in this article reflect the results of research conducted by the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or United States Government.

Conflicts of Interest

The authors have no other conflicts to disclose.

Ethical Approval/Animal Rights

This study complies with all ethical guidelines and was conducted with approval and supervision of the institutional animal care and use committee.

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This article is part of the collection “Spreading Cortical Depolarization.”

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Hartings, J.A., Carroll, C.P. & Lee, G. Spreading Diffusion-Restriction Events in the Gyrencephalic Brain After Subarachnoid Hemorrhage Revealed by Continuous Magnetic Resonance Imaging. Neurocrit Care 37 (Suppl 1), 60–66 (2022). https://doi.org/10.1007/s12028-021-01376-0

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  • DOI: https://doi.org/10.1007/s12028-021-01376-0

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