journal article·2024-09-20Open access

Cortical Connectivity Response to Hyperventilation in Focal Epilepsy: A Stereo-EEG Study

Lorenzo Ferri, Federico Mason, Lidia Di Vito, Elena Pasini, Roberto Michelucci, Francesco Cardinale, Roberto Mai, Lara Alvisi, Luca Zanuttini, Matteo Martinoni, Francesca Bisulli

Applied Sciences· Volume 14· Issue 18

Abstract

Hyperventilation (HV) is an activation technique performed during clinical practices to trigger epileptiform activities, supporting the neurophysiological evaluation of patients with epilepsy. Although the role of HV has often been questioned, especially in the case of focal epilepsy, no studies have ever assessed how cortical structures respond to such a maneuver via intracranial EEG recordings. This work aims to fill this gap by evaluating the HV effects on the Stereo-EEG (SEEG) signals from a cohort of 10 patients with drug-resistant focal epilepsy. We extracted multiple quantitative metrics from the SEEG signals and compared the results obtained during HV, awake status, non-REM sleep, and seizure onset. Our findings show that the cortical connectivity, estimated via the phase transfer entropy (PTE) algorithm, strongly increases during the HV maneuver, similar to non-REM sleep. The opposite effect is observed during seizure onset, as ictal transitions involve the desynchronization of the brain structures within the epileptogenic zone. We conclude that HV promotes a conductive environment that may facilitate the propagation of epileptiform activities but is not sufficient to trigger seizures in focal epilepsy.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Functional Brain Connectivity Studies · Neural dynamics and brain function · EEG and Brain-Computer Interfaces

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

IRCCS Istituto delle Scienze Neurologiche di Bologna, Full Member of the European Reference Network EpiCARE, 40139 Bologna, Italy

Department of Neuromotor and Biomedical Sciences, University of Bologna, 40127 Bologna, Italy

Department of Information Engineering, University of Padova, 35131 Padova, Italy

Centro Munari Chirurgia dell’Epilessia e del Parkinson, Niguarda Hospital, 20162 Milan, Italy

Unit of Neuroscience, Department of Medicine and Surgery, University of Parma, 43124 Parma, Italy

References (33)

Show source-provided references
1. Hyperventilation during electroencephalography: Safety and efficacy10.1016/j.seizure.2013.10.010 ↗
2. Zur Pathogenese und chirurgischen Behandlung der Epilepsie
3. The electro-encephalogram in diagnosis and in localization of epileptic seizures10.1001/archneurpsyc.1936.02260120072005 ↗
4. Effect of hyperventilation on electroencephalographic activity
5. Response of human epileptic temporal lobe cortical blood flow to hyperventilation10.1016/0920-1211(95)00021-2 ↗
6. Response of medullary respiratory neurons to hypercapnia and isocapnic hypoxia10.1152/jappl.1977.43.5.812 ↗
7. Hyperventilation induces sympathetic overactivation in mesial temporal epilepsy10.1016/j.eplepsyres.2014.12.003 ↗
8. Hyperventilation and Seizures: Not a New sense: A Literature review10.1055/s-0043-1774808 ↗
9. Mason, F., Scarabello, A., Taruffi, L., Pasini, E., Calandra-Buonaura, G., Vignatelli, L., and Bisulli, F. (2024). Heart Rate Variability as a Tool for Seizure Prediction: A Scoping Review. J. Clin. Med., 13.10.3390/jcm13030747 ↗
10. Does hyperventilation elicit epileptic seizures?10.1111/j.0013-9580.2004.63803.x ↗
11. Hyperventilation revisited: Physiological effects and efficacy on focal seizure activation in the era of video-EEG monitoring10.1111/j.0013-9580.2005.11104.x ↗
12. Li, Z., Hwang, K., Li, K., Wu, J., and Ji, T. (2022). Graph-generative neural network for EEG-based epileptic seizure detection via discovery of dynamic brain functional connectivity. Sci. Rep., 12.10.1038/s41598-022-23656-1 ↗
13. Review of advanced techniques for the estimation of brain connectivity measured with EEG/MEG10.1016/j.compbiomed.2011.06.020 ↗
14. Phase transfer entropy: A novel phase-based measure for directed connectivity in networks coupled by oscillatory interactions10.1016/j.neuroimage.2013.08.056 ↗
15. Hyperventilation in Patients with Focal Epilepsy: Electromagnetic Tomography, Functional Connectivity and Graph Theory—A Possible Tool in Epilepsy Diagnosis?10.1097/WNP.0000000000000329 ↗
16. Advances in human intracranial electroencephalography research, guidelines and good practices10.1016/j.neuroimage.2022.119438 ↗
17. Lesion, “irritative” zone and epileptogenic focus10.1159/000103937 ↗
18. Stereoelectroencephalography: Surgical methodology, safety, and stereotactic application accuracy in 500 procedures10.1227/NEU.0b013e31827d1161 ↗
19. Greene, P., Li, A., González-Martínez, J., and Sarma, S.V. (2021). Classification of stereo-EEG contacts in white matter vs. Gray matter using recorded activity. Front. Neurol., 11.10.3389/fneur.2020.605696 ↗
20. A multivariate comparison between two EEG analysis techniques: Period analysis and fast Fourier transform10.1016/0013-4694(81)91441-3 ↗
21. Epileptogenicity of brain structures in human temporal lobe epilepsy: A quantified study from intracerebral EEG10.1093/brain/awn111 ↗
22. Sturges’ rule10.1002/wics.35 ↗
23. Analysis of epileptic EEG signals using higher order spectra10.1080/03091900701559408 ↗
24. De Clercq, W., Lemmerling, P., Van Paesschen, W., and Van Huffel, S. (2003, January 17–21). Characterization of interictal and ictal scalp EEG signals with the Hilbert transform. Proceedings of the 25th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Cancún, Mexico.
25. Chiarion, G., Sparacino, L., Antonacci, Y., Faes, L., and Mesin, L. (2023). Connectivity analysis in EEG data: A tutorial review of the state of the art and emerging trends. Bioengineering, 10.10.3390/bioengineering10030372 ↗
26. Functional and effective connectivity in neuroimaging: A synthesis10.1002/hbm.460020107 ↗
27. Best practice in statistics: Use the Welch t-test when testing the difference between two groups10.1177/0004563221992088 ↗
28. Edakawa, K., Yanagisawa, T., Kishima, H., Fukuma, R., Oshino, S., Khoo, H.M., Kobayashi, M., Tanaka, M., and Yoshimine, T. (2016). Detection of epileptic seizures using phase–amplitude coupling in intracranial electroencephalography. Sci. Rep., 6.10.1038/srep25422 ↗
29. Mason, F., Ferri, L., Vito, L.D., Alvisi, L., Zanuttini, L., Martinoni, M., Mai, R., Cardinale, F., Tinuper, P., and Michelucci, R. (2024). Desynchronization Index: A New Approach for Exploring Complex Epileptogenic Networks in Stereoelectroencephalography. arXiv.
30. Sleep and epilepsy: A snapshot of knowledge and future research lines10.1111/jsr.13622 ↗
31. Grouping of brain rhythms in corticothalamic systems10.1016/j.neuroscience.2005.10.029 ↗
32. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves10.1093/brain/awv073 ↗
33. Interictal spiking during wakefulness and sleep and the localization of foci in temporal lobe epilepsy10.1212/WNL.41.2_Part_1.290 ↗