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Brain 2007 130(4):995-1008; doi:10.1093/brain/awl392
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© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex

Anthony J. Strong1, Peter J. Anderson1, Helena R. Watts1, David J. Virley2, Andrew Lloyd2, Elaine A. Irving2, Toshiaki Nagafuji2, Mitsuyoshi Ninomiya2, Hajime Nakamura4, Andrew K. Dunn3 and Rudolf Graf4

1King's College London, Department of Clinical Neurosciences (Neurosurgery), UK, 2Shionogi-GlaxoSmithKline LLC, 3University of Texas at Austin, Biomedical Engineering, Austin, TX, USA and 4Max-Planck Institute for Neurological Research, Cologne, Germany

Correspondence to: Prof. Anthony J. Strong, Department of Neurosurgery, King's College Hospital, London SE5 9RS, UK E-mail: anthony.strong{at}kcl.ac.uk

In the light of accumulating evidence for the occurrence of spontaneous cortical spreading depression and peri-infarct depolarizations in the human brain injured by trauma or aneurysmal subarachnoid haemorrhage, we used DC electrode recording and laser speckle imaging to study the relationship between depolarization events and perfusion in the ischaemic, gyrencephalic brain. In 14 adult male cats anaesthetized with chloralose, one cerebral hemisphere was exposed and the middle cerebral artery occluded. Surface cortical perfusion in core and penumbral territories was imaged semiquantitatively at intervals of 13 s for 4 h. Cortical surface DC potential was recorded. Time interval between changes in DC potential and in perfusion was examined, and this comparison was repeated using microelectrodes for DC potential in five similar experiments in a second laboratory. Mean pre-occlusion perfusion was 11707 ± 4581 units (equivalent to CBF (cerebral blood flow) ~40.5 ± SD 14.4 ml/100 g/min), and fell on occlusion to 5318 ± 2916 (CBF ~17.1 ± 8.3), 5291 ± 3407 (CBF ~17.0 ± 10.1), and 6711 ± 3271 (CBF ~22.2 ± 9.6), quickly recovering to 8704 ± 4581 (CBF ~29.5 ± 14.4), 9741 ± 4499 (CBF ~33.3 ± 14.1) and 10 314 ± 3762 (CBF ~35.4 ± 11.4) on the core, intermediate and outer penumbral gyri, respectively. Mean perfusion later fell secondarily on core and intermediate gyri but, overall, was preserved on the outer (upper level of perfusion) gyrus during the period of observation. Pattern and severity of transient changes in perfusion associated with depolarization events varied with gyral location; falls in perfusion were sometimes profound and irreversible, and followed rather than preceded depolarization. In this model of occlusive stroke, reductions in perfusion linked to peri-infarct depolarization events contribute to secondary deterioration in penumbral areas. The findings suggest that such events play a central rather than a subsidiary role in cerebral infarction in the gyrencephalic brain.

Key Words: penumbra; depolarization; spreading cortical depression; laser speckle imaging; middle cerebral artery occlusion

Abbreviations: CSD, cortical spreading depression; CBF, cerebral blood flow; ECoG, electrocorticographic; EG, ectosylviangyrus; MAP, mean arterial pressure; MCAO, middle cerebral artery occlusion; MG, marginalgyrus; PIDs, peri-infarct depolarizations; SAH, subarachnoid haemorrhage; SG, suprasylviangyrus

Received June 22, 2006. Revised November 15, 2006. Second revision on December 18, 2006. Accepted December 22, 2006.


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