Background: We present a compelling case fitting the phenomenon of cortical spreading depression detected by intraoperative neurophysiological monitoring (IONM) following an intraoperative seizure during a craniotomy for revascularization. Cortical spreading depression (CSD, also called cortical spreading depolarization) is a pathophysiological phenomenon whereby a wave of depolarization is thought to propagate across the cerebral cortex, creating a brief period of relative neuronal inactivity. The relationship between CSD and seizures is unclear, although some literature has made a correlation between seizures and a cortical environment conducive to CSD. Methods: Intraoperative somatosensory evoked potentials (SSEPs) and electroencephalography (EEG) were monitored continuously during the craniotomy procedure utilizing standard montages. Electrophysiological data from pre-ictal, ictal, and post-ictal periods were recorded. Results: During the procedure, intraoperative EEG captured a generalized seizure followed by a stepwise decrease in somatosensory evoked potential cortical amplitudes, compelling for the phenomenon of CSD. The subsequent partial recovery of neuronal function was also captured electrophysiologically. Discussion: While CSD is considered controversial in some aspects, intraoperative neurophysiological monitoring allowed for the unique analysis of a case demonstrating a CSD-like phenomenon. To our knowledge, this is the first published example of this phenomenon in which intraoperative neurophysiological monitoring captured a seizure, along with a stepwise subsequent reduction in SSEP cortical amplitudes not explained by other variables.
References
[1]
Leao, A.A.P. (1944) Spreading Depression of Activity in the Cerebral Cortex. Journal of Neurophysiology, 7, 359-390. https://doi.org/10.1152/jn.1944.7.6.359
[2]
Stafstrom, C.E. (2020) Stopped at the Border: Cortical Spreading Depolarization Blocks Seizure Propagation. Epilepsy Currents, 20, 171-172. https://doi.org/10.1177/1535759720916448
[3]
Zakharov, A., Chernova, K., Burkhanova, G., Holmes, G.L. and Khazipov, R. (2019) Segregation of Seizures and Spreading Depolarization across Cortical Layers. Epilepsia, 60, 2386-2397. https://doi.org/10.1111/epi.16390
[4]
Dreier, J.P. and Reiffurth, C. (2015) The Stroke-Migraine Depolarization Continuum. Neuron, 86, 902-922. https://doi.org/10.1016/j.neuron.2015.04.004
[5]
Bouley, J., Chung, D.Y., Ayata, C., Brown, R.H. and Henninger, N. (2019) Cortical Spreading Depression Denotes Concussion Injury. Journal of Neurotrauma, 36, 1008-1017. https://doi.org/10.1089/neu.2018.5844
[6]
Bogdanov, V.B., Multon, S., Chauvel, V., Bogdanova, O.V., Prodanov, D., Makarchuk, M.Y., et al. (2011) Migraine Preventive Drugs Differentially Affect Cortical Spreading Depression in Rat. Neurobiology of Disease, 41, 430-435. https://doi.org/10.1016/j.nbd.2010.10.014
[7]
Ringuette, D., EbrahimAmini, A., Sangphosuk, W., Aquilino, M.S., Carroll, G., Ashley, M., et al. (2024) Spreading Depolarization Suppression from Inter-Astrocytic Gap Junction Blockade Assessed with Multimodal Imaging and a Novel Wavefront Detection Scheme. Neurotherapeutics, 21, e00298. https://doi.org/10.1016/j.neurot.2023.10.008
[8]
Kramer, D.R., Fujii, T., Ohiorhenuan, I. and Liu, C.Y. (2017) Interplay between Cortical Spreading Depolarization and Seizures. Stereotactic and Functional Neurosurgery, 95, 1-5. https://doi.org/10.1159/000452841
[9]
Pottkämper, J.C.M., Hofmeijer, J., van Waarde, J.A. and van Putten, M.J.A.M. (2020) The Postictal State—What Do We Know? Epilepsia, 61, 1045-1061. https://doi.org/10.1111/epi.16519
[10]
Seyal, M., Bateman, L.M. and Li, C. (2012) Impact of Periictal Interventions on Respiratory Dysfunction, Postictal EEG Suppression, and Postictal Immobility. Epilepsia, 54, 377-382. https://doi.org/10.1111/j.1528-1167.2012.03691.x
[11]
Beniczky, S., Jovanovic, M., Atkins, M.D., Alving, J., Dahl, M., Andersen, N., et al. (2010) Postictal Inhibition of the Somatosensory Cortex. Neurological Sciences, 32, 147-149. https://doi.org/10.1007/s10072-010-0362-x
[12]
Diaczun, C. and Lüders, H.O. (2019) Waveform Window #45: Cortical Amplitude Reduction of Somatosensory Evoked Potentials during Epileptic Seizure. The Neurodiagnostic Journal, 59, 169-177. https://doi.org/10.1080/21646821.2019.1618087
[13]
Charles, A. and Brennan, K. (2009) Cortical Spreading Depression—New Insights and Persistent Questions. Cephalalgia, 29, 1115-1124. https://doi.org/10.1111/j.1468-2982.2009.01983.x
[14]
Vitale, M., Tottene, A., Zarin Zadeh, M., Brennan, K. and Pietrobon, D. (2023) Mechanisms of Initiation of Cortical Spreading Depression. The Journal of Headache and Pain, 24, Article No. 105. https://doi.org/10.1186/s10194-023-01643-9
[15]
Arkilo, D., Wang, S. and Thiele, E.A. (2013) Time Interval Required for Return to Baseline of the Background Rhythm on Electroencephalogram after Recorded Electrographic Seizures. Epilepsy Research, 106, 288-291. https://doi.org/10.1016/j.eplepsyres.2013.04.007
[16]
Abou-Khalil, B. (2008) Levetiracetam in the Treatment of Epilepsy. Neuropsychiatric Disease and Treatment, 4, 507-523. https://doi.org/10.2147/ndt.s2937
[17]
Blume, W.T. (2006) Drug Effects on EEG. Journal of Clinical Neurophysiology, 23, 306-311. https://doi.org/10.1097/01.wnp.0000229137.94384.fa
