Phase-Amplitude Coupling Localizes Pathologic Brain with Aid of Behavioral Staging in Sleep
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
37240831
PubMed Central
PMC10221792
DOI
10.3390/life13051186
PII: life13051186
Knihovny.cz E-zdroje
- Klíčová slova
- behavioral staging, epilepsy, phase-amplitude coupling (PAC),
- Publikační typ
- časopisecké články MeSH
Low frequency brain rhythms facilitate communication across large spatial regions in the brain and high frequency rhythms are thought to signify local processing among nearby assemblies. A heavily investigated mode by which these low frequency and high frequency phenomenon interact is phase-amplitude coupling (PAC). This phenomenon has recently shown promise as a novel electrophysiologic biomarker, in a number of neurologic diseases including human epilepsy. In 17 medically refractory epilepsy patients undergoing phase-2 monitoring for the evaluation of surgical resection and in whom temporal depth electrodes were implanted, we investigated the electrophysiologic relationships of PAC in epileptogenic (seizure onset zone or SOZ) and non-epileptogenic tissue (non-SOZ). That this biomarker can differentiate seizure onset zone from non-seizure onset zone has been established with ictal and pre-ictal data, but less so with interictal data. Here we show that this biomarker can differentiate SOZ from non-SOZ interictally and is also a function of interictal epileptiform discharges. We also show a differential level of PAC in slow-wave-sleep relative to NREM1-2 and awake states. Lastly, we show AUROC evaluation of the localization of SOZ is optimal when utilizing beta or alpha phase onto high-gamma or ripple band. The results suggest an elevated PAC may reflect an electrophysiology-based biomarker for abnormal/epileptogenic brain regions.
Department of Neurology Mayo Clinic Rochester MN 55905 USA
Department of Physiology and Biomedical Engineering Mayo Clinic Rochester MN 55905 USA
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Fisher R.S., Acevedo C., Arzimanoglou A., Bogacz A., Cross J.H., Elger C.E., Engel J., Jr., Forsgren L., French J.A., Glynn M., et al. ILAE official report: A practical clinical definition of epilepsy. Epilepsia. 2014;55:475–482. doi: 10.1111/epi.12550. PubMed DOI
Banerjee P.N., Filippi D., Hauser W.A. The Descriptive Epidemiology of Epilepsy-a Review. Epilepsy Res. 2009;85:31–45. doi: 10.1016/j.eplepsyres.2009.03.003. PubMed DOI PMC
Geertsema E.E., Visser G.H., Velis D.N., Claus S.P., Zijlmans M., Kalitzin S. Automated Seizure Onset Zone Approximation Based on Nonharmonic High-Frequency Oscillations in Human Interictal Intracranial EEGs. Int. J. Neural Syst. 2015;25:1550015. doi: 10.1142/S012906571550015X. PubMed DOI
Kremen V., Duque J.J., Brinkmann B.H., Berry B.M., Kucewicz M.T., Khadjevand F., Van Gompel J., Stead M., Louis E.K.S., Worrell G.A. Behavioral State Classification in Epileptic Brain Using Intracranial Electrophysiology. J. Neural Eng. 2017;14:26001. doi: 10.1088/1741-2552/aa5688. PubMed DOI PMC
Novikov E., Novikov A., Shannahoff-Khalsa D., Schwartz B., Wright J. Scale-similar activity in the brain. Phys. Rev. E. 1997;56:R2387–R2389. doi: 10.1103/PhysRevE.56.R2387. DOI
Saboo K.V., Varatharajah Y., Berry B.M., Kremen V., Sperling M.R., Davis K.A., Jobst B.C., Gross R.E., Lega B., Sheth S.A., et al. Unsupervised machine-learning classification of electrophysiologically active electrodes during human cognitive task performance. Sci. Rep. 2019;9:17390. doi: 10.1038/s41598-019-53925-5. PubMed DOI PMC
Wagh N., Wei J., Rawal S., Berry B.M., Barnard L., Brinkmann B.H., Worrell G.A., Jones D.T., Varatharajah Y. Domain-guided Self-supervision of EEG Data Improves Downstream Classification Performance and Generalizability; Proceedings of the Machine Learning Research (PMLR); Virtual Event. 6–7 August 2021.
Varatharajah Y., Chong M.J., Saboo K.V., Berry B.M., Brinkmann B.H., Worrell G.A., Iyer R.K. EEG-GRAPH: A Factor-Graph-Based Model for Capturing Spatial, Temporal, and Observational Relationships in Electroencephalograms. NIPS; Denver, CO, USA: 2017.
Varatharajah Y., Berry B., Joseph B., Balzekas I., Attia T.P., Kremen V., Brinkmann B., Iyer R., Worrell G. Characterizing the electrophysiological abnormalities in visually reviewed normal EEGs of drug-resistant focal epilepsy patients. Brain Commun. 2021;3:fcab102. doi: 10.1093/braincomms/fcab102. PubMed DOI PMC
Matsumoto A., Brinkmann B.H., Stead S.M., Matsumoto J., Kucewicz M.T., Marsh W.R., Meyer F., Worrell G. Pathological and Physiological High-Frequency Oscillations in Focal Human Epilepsy. J. Neurophysiol. 2013;110:1958–1964. doi: 10.1152/jn.00341.2013. PubMed DOI PMC
Burns S.P., Santaniello S., Yaffe R.B., Jouny C.C., Crone N.E., Bergey G.K., Anderson W.S., Sarma S.V. Network dynamics of the brain and influence of the epileptic seizure onset zone. Proc. Natl. Acad. Sci. USA. 2014;111:E5321–E5330. doi: 10.1073/pnas.1401752111. PubMed DOI PMC
Alvarado-Rojas C., Valderrama M., Fouad-Ahmed A., Feldwisch-Drentrup H., Ihle M., Teixeira C.A., Sales F., Schulze-Bonhage A., Adam C., Dourado A., et al. Slow Modulations of High-Frequency Activity (40–140 Hz) Discriminate Preictal Changes in Human Focal Epilepsy. Sci. Rep. 2014;4:4545. doi: 10.1038/srep04545. PubMed DOI PMC
Edakawa K., Yanagisawa T., Kishima H., Fukuma R., Oshino S., Khoo H.M., Kobayashi M., Tanaka M., Yoshimine T. Detection of Epileptic Seizures Using Phase–Amplitude Coupling in Intracranial Electroencephalography. Sci. Rep. 2016;6:25422. doi: 10.1038/srep25422. PubMed DOI PMC
Kucewicz M.T., Berry B.M., Miller L.R., Khadjevand F., Ezzyat Y., Stein J.M., Kremen V., Brinkmann B.H., Wanda P., Sperling M.R., et al. Dissecting Gamma Frequency Activity during Human Memory Processing. Brain. 2017;140:1337–1350. doi: 10.1093/brain/awx043. PubMed DOI
Kucewicz M.T., Cimbalnik J., Matsumoto J.Y., Brinkmann B.H., Bower M.R., Vasoli V., Sulc V., Meyer F., Marsh W.R., Stead S.M., et al. High Frequency Oscillations Are Associated with Cognitive Processing in Human Recognition Memory. Pt 8Brain A J. Neurol. 2014;137:2231–2244. doi: 10.1093/brain/awu149. PubMed DOI PMC
Kucewicz M.T., Berry B.M., Bower M.R., Cimbalnik J., Svehlik V., Stead S.M., Worrell G.A. Combined Single Neuron Unit Activity and Local Field Potential Oscillations in a Human Visual Recognition Memory Task. IEEE Trans. Biomed. Eng. 2016;63:67–75. doi: 10.1109/TBME.2015.2451596. PubMed DOI
Weiss S.A., Lemesiou A., Connors R., Banks G.P., McKhann G.M., Goodman R.R., Zhao B., Filippi C.G., Nowell M., Rodionov R., et al. Seizure Localization Using Ictal Phase-Locked High Gamma: A Retrospective Surgical Outcome Study. Neurology. 2015;84:2320–2328. doi: 10.1212/WNL.0000000000001656. PubMed DOI PMC
Weiss S.A., Orosz I., Salamon N., Moy S., Wei L., Klooster M.A.V., Knight R.T., Harper R.M., Bragin A., Fried I., et al. Ripples on Spikes Show Increased Phase-Amplitude Coupling in Mesial Temporal Lobe Epilepsy Seizure-Onset Zones. Epilepsia. 2016;57:1916–1930. doi: 10.1111/epi.13572. PubMed DOI PMC
Canolty R.T., Edwards E., Dalal S.S., Soltani M., Nagarajan S.S., Kirsch H.E., Berger M.S., Barbaro N.M., Knight R.T. High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex. Science. 2006;313:1626–1628. doi: 10.1126/science.1128115. PubMed DOI PMC
Jacobs J., Vogt C., LeVan P., Zelmann R., Gotman J., Kobayashi K. The Identification of Distinct High-Frequency Oscillations during Spikes Delineates the Seizure Onset Zone Better than High-Frequency Spectral Power Changes. Clin. Neurophysiol. 2016;127:129–142. doi: 10.1016/j.clinph.2015.04.053. PubMed DOI
Buzsáki G., Draguhn A. Neuronal oscillations in cortical networks. Science. 2004;304:1926–1929. doi: 10.1126/science.1099745. PubMed DOI
Linkenkaer-Hansen K., Nikouline V.V., Palva J.M., Ilmoniemi R.J. Long-range temporal correlations and scaling behavior in human brain oscillations. J. Neurosci. 2001;21:1370–1377. doi: 10.1523/JNEUROSCI.21-04-01370.2001. PubMed DOI PMC
Vanhatalo S., Palva J.M., Holmes M.D., Miller J.W., Voipio J., Kaila K. Infraslow Oscillations Modulate Excitability and Interictal Epileptic Activity in the Human Cortex during Sleep. Proc. Natl. Acad. Sci. USA. 2004;101:5053–5057. doi: 10.1073/pnas.0305375101. PubMed DOI PMC
Monto S., Palva S., Voipio J., Palva J.M. Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J. Neurosci. 2008;28:8268–8272. doi: 10.1523/JNEUROSCI.1910-08.2008. PubMed DOI PMC
Canolty R.T., Knight R.T. The Functional Role of Cross-Frequency Coupling. Trends Cogn. Sci. 2010;14:506–515. doi: 10.1016/j.tics.2010.09.001. PubMed DOI PMC
Osipova D., Hermes D., Jensen O. Gamma Power Is Phase-Locked to Posterior Alpha Activity. PLoS ONE. 2008;3:e3990. doi: 10.1371/journal.pone.0003990. PubMed DOI PMC
Amiri M., Frauscher B., Gotman J. Phase-Amplitude Coupling Is Elevated in Deep Sleep and in the Onset Zone of Focal Epileptic Seizures. Front. Hum. Neurosci. 2016;10:387. doi: 10.3389/fnhum.2016.00387. PubMed DOI PMC
Mihály I., Orbán-Kis K., Gáll Z., Berki Á.-J., Bod R.-B., Szilágyi T. Amygdala Low-Frequency Stimulation Reduces Pathological Phase-Amplitude Coupling in the Pilocarpine Model of Epilepsy. Brain Sci. 2020;10:856. doi: 10.3390/brainsci10110856. PubMed DOI PMC
Pasquetti M.V., Meier L., Marafiga J.R., Caus L.B., Tort A.B.L., Calcagnotto M.E. Hippocampal CA1 and cortical interictal oscillations in the pilocarpine model of epilepsy. Brain Res. 2019;1722:146351. doi: 10.1016/j.brainres.2019.146351. PubMed DOI
Samiee S., Lévesque M., Avoli M., Baillet S. Phase-amplitude coupling and epileptogenesis in an animal model of mesial temporal lobe epilepsy. Neurobiol. Dis. 2018;114:111–119. doi: 10.1016/j.nbd.2018.02.008. PubMed DOI PMC
Guirgis M., Chinvarun Y., del Campo M., Carlen P.L., Bardakjian B.L. Defining Regions of Interest Using Cross-Frequency Coupling in Extratemporal Lobe Epilepsy Patients. J. Neural Eng. 2015;12:26011. doi: 10.1088/1741-2560/12/2/026011. PubMed DOI
Ibrahim G.M., Wong S.M., Anderson R.A., Singh-Cadieux G., Akiyama T., Ochi A., Otsubo H., Okanishi T., Valiante T.A., Donner E., et al. Dynamic Modulation of Epileptic High Frequency Oscillations by the Phase of Slower Cortical Rhythms. Exp. Neurol. 2014;251:30–38. doi: 10.1016/j.expneurol.2013.10.019. PubMed DOI
Maris E., van Vugt M., Kahana M. Spatially Distributed Patterns of Oscillatory Coupling between High-Frequency Amplitudes and Low-Frequency Phases in Human iEEG. NeuroImage. 2011;54:836–850. doi: 10.1016/j.neuroimage.2010.09.029. PubMed DOI
Staresina B.P., Bergmann T.O., Bonnefond M., Van Der Meij R., Jensen O., Deuker L., Elger C.E., Axmacher N., Fell J. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat. Neurosci. 2015;18:1679–1686. doi: 10.1038/nn.4119. PubMed DOI PMC
Achermann P., Borbély A.A. Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience. 1997;81:213–222. PubMed
Steriade M., Nunez A. Oscillatory Processes in the Brain. CRC Press; Boca Raton, FL, USA: 1993.
Sirota A., Csicsvari J., Buhl D., Buzsáki G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. USA. 2003;100:2065–2069. doi: 10.1073/pnas.0437938100. PubMed DOI PMC
Andrillon T., Nir Y., Staba R.J., Ferrarelli F., Cirelli C., Tononi G., Fried I. Sleep spindles in humans: Insights from intracranial EEG and unit recordings. J. Neurosci. 2011;31:17821–17834. doi: 10.1523/JNEUROSCI.2604-11.2011. PubMed DOI PMC
Roebber J.K., Lewis P.A., Crunelli V., Navarrete M., Hamandi K. Effects of Anti-Seizure Medication on Sleep Spindles and Slow Waves in Drug-Resistant Epilepsy. Brain Sci. 2022;12:1288. doi: 10.3390/brainsci12101288. PubMed DOI PMC
Gouveris H., Koirala N., Anwar A.R., Ding H., Ludwig K., Huppertz T., Matthias C., Groppa S., Muthuraman M. Reduced Cross-Frequency Coupling and Daytime Sleepiness in Obstructive Sleep Apnea Patients. Biology. 2022;11:700. doi: 10.3390/biology11050700. PubMed DOI PMC
Diekelmann S., Born J. The Memory Function of Sleep. Nat. Rev. Neurosci. 2010;11:114–126. doi: 10.1038/nrn2762. PubMed DOI
Varatharajah Y., Berry B.M., Kalbarczyk Z.T., Brinkmann B.H., Worrell G.A., Iyer R.K. Inter-ictal Seizure Onset Zone localization using unsupervised clustering and Bayesian Filtering; Proceedings of the 2017 8th International IEEE/EMBS Conference on Neural Engineering (NER); Shanghai, China. 25–28 May 2017; pp. 533–539.
Thompson G.J., Pan W.-J., Billings J.C.W., Grooms J.K., Shakil S., Jaeger D., Keilholz S.D. Phase-Amplitude Coupling and Infraslow. Front. Integr. Neurosci. 2014;8:41. doi: 10.3389/fnint.2014.00041. PubMed DOI PMC
Thompson S.A., Krishnan B., Gonzalez-Martinez J., Bulacio J., Jehi L., Mosher J., Alexopoulos A., Burgess R.C. Interictal Infraslow Activity in Stereoelectroencephalography. J. Clin. Neurophysiol. 2016;33:141–148. doi: 10.1097/WNP.0000000000000236. PubMed DOI
Ren L., Kucewicz M.T., Cimbalnik J., Matsumoto J.Y., Brinkmann B.H., Hu W., Marsh W.R., Meyer F.B., Stead S.M., Worrell G.A. Gamma Oscillations Precede Interictal Epileptiform Spikes in the Seizure Onset Zone. Neurology. 2015;84:602–608. doi: 10.1212/WNL.0000000000001234. PubMed DOI PMC
Bower M.R., Stead M., Bower R.S., Kucewicz M.T., Sulc V., Cimbalnik J., Brinkmann B.H., Vasoli V.M., Louis E.K.S., Meyer F.B., et al. Evidence for Consolidation of Neuronal Assemblies after Seizures in Humans. J. Neurosci. 2015;35:999–1010. doi: 10.1523/JNEUROSCI.3019-14.2015. PubMed DOI PMC
Brinkmann B.H., Bower M.R., Stengel K.A., Worrell G.A., Stead M. Large-scale electrophysiology: Acquisition, compression, encryption, and storage of big data. J. Neurosci. Methods. 2009;180:185–192. doi: 10.1016/j.jneumeth.2009.03.022. PubMed DOI PMC
Barkmeier D.T., Shah A.K., Flanagan D., Atkinson M.D., Agarwal R., Fuerst D.R., Jafari-Khouzani K., Loeb J.A. High Inter-Reviewer Variability of Spike Detection on Intracranial EEG Addressed by an Automated Multi-Channel Algorithm. Clin. Neurophysiol. 2012;123:1088–1095. doi: 10.1016/j.clinph.2011.09.023. PubMed DOI PMC
Cimbalnik J., Kucewicz M., Worrell G. Interictal High-Frequency Oscillations in Focal Human Epilepsy. Curr. Opin. Neurol. 2016;29:175–181. doi: 10.1097/WCO.0000000000000302. PubMed DOI PMC
Jordan D., Ilg R., Riedl V., Schorer A., Grimberg S., Neufang S., Omerovic A., Berger S., Untergehrer G., Preibisch C., et al. Simultaneous electroencephalographic and functional magnetic resonance imaging indicate impaired cortical top-down processing in association with anesthetic-induced unconsciousness. Anesthesiology. 2013;119:1031–1042. doi: 10.1097/ALN.0b013e3182a7ca92. PubMed DOI
Bagshaw A.P., Jacobs J., LeVan P., Dubeau F., Gotman J. Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy. Epilepsia. 2009;50:617–628. doi: 10.1111/j.1528-1167.2008.01784.x. PubMed DOI PMC
Valencia M., Artieda J., Bolam J.P., Mena-Segovia J. Dynamic interaction of spindles and gamma activity during cortical slow oscillations and its modulation by subcortical afferents. PLoS ONE. 2013;8:e67540. doi: 10.1371/journal.pone.0067540. PubMed DOI PMC
Demuru M., Kalitzin S., Zweiphenning W., van Blooijs D., Klooster M.V., Van Eijsden P., Leijten, F., Zijlmans M., Braun K., Ferrier C., et al. The value of intra-operative electrographic biomarkers for tailoring during epilepsy surgery: From group-level to patient-level analysis. Sci. Rep. 2020;10:14654. doi: 10.1038/s41598-020-71359-2. PubMed DOI PMC
Cámpora N.E., Mininni C.J., Kochen S., Lew S.E. Seizure localization using pre ictal phase-amplitude coupling in intracranial electroencephalography. Sci. Rep. 2019;9:20022. doi: 10.1038/s41598-019-56548-y. PubMed DOI PMC
Bandarabadi M., Gast H., Rummel C., Bassetti C., Adamantidis A., Schindler K., Zubler F. Assessing Epileptogenicity Using Phase-Locked High Frequency Oscillations: A Systematic Comparison of Methods. Front. Neurol. 2019;10:1132. doi: 10.3389/fneur.2019.01132. PubMed DOI PMC
Mukamel E.A., Wong K.F., Prerau M.J., Brown E.N., Purdon P.L. Phase-Based Measures of Cross-Frequency Coupling in Brain Electrical Dynamics under General Anesthesia; Proceedings of the 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society; Boston, MA, USA. 30 August–3 September 2011; pp. 1981–1984. PubMed DOI PMC
Mukamel E.A., Pirondini E., Babadi B., Wong K.F.K., Pierce E.T., Harrell P.G., Walsh J.L., Salazar-Gomez A.F., Cash S.S., Eskandar E.N., et al. A Transition in Brain State during Propofol-Induced Unconsciousness. J. Neurosci. 2014;34:839–845. doi: 10.1523/JNEUROSCI.5813-12.2014. PubMed DOI PMC
Geertsema E.E., Klooster M.A.V., van Klink N.E., Leijten F.S., van Rijen P.C., Visser G.H., Kalitzin S.N., Zijlmans M. Non-Harmonicity in High-Frequency Components of the Intra-Operative Corticogram to Delineate Epileptogenic Tissue during Surgery. Clin. Neurophysiol. 2017;128:153–164. doi: 10.1016/j.clinph.2016.11.007. PubMed DOI
Guragain H., Cimbalnik J., Stead M., Groppe D.M., Berry B.M., Kremen V., Kenney-Jung D., Britton J., Worrell G.A., Brinkmann B.H. Spatial variation in high-frequency oscillation rates and amplitudes in intracranial EEG. Neurology. 2018;90:e639–e646. doi: 10.1212/WNL.0000000000004998. PubMed DOI PMC
Iber C., Ancoli-Israel S., Chesson A., Quan S.F. For the American Academy of Sleep Medicine. The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. American Academy of Sleep Medicine; Westchester, IL, USA: 2007.