Leveraging electrophysiologic correlates of word encoding to map seizure onset zone in focal epilepsy: Task-dependent changes in epileptiform activity, spectral features, and functional connectivity

. 2021 Nov ; 62 (11) : 2627-2639. [epub] 20210918

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid34536230

Grantová podpora
UH2 NS095495 NINDS NIH HHS - United States
UH3 NS095495 NINDS NIH HHS - United States
T32 GM065841 NIGMS NIH HHS - United States
R01 NS092882 NINDS NIH HHS - United States

OBJECTIVE: Verbal memory dysfunction is common in focal, drug-resistant epilepsy (DRE). Unfortunately, surgical removal of seizure-generating brain tissue can be associated with further memory decline. Therefore, localization of both the circuits generating seizures and those underlying cognitive functions is critical in presurgical evaluations for patients who may be candidates for resective surgery. We used intracranial electroencephalographic (iEEG) recordings during a verbal memory task to investigate word encoding in focal epilepsy. We hypothesized that engagement in a memory task would exaggerate local iEEG feature differences between the seizure onset zone (SOZ) and neighboring tissue as compared to wakeful rest ("nontask"). METHODS: Ten participants undergoing presurgical iEEG evaluation for DRE performed a free recall verbal memory task. We evaluated three iEEG features in SOZ and non-SOZ electrodes during successful word encoding and compared them with nontask recordings: interictal epileptiform spike (IES) rates, power in band (PIB), and relative entropy (REN; a functional connectivity measure). RESULTS: We found a complex pattern of PIB and REN changes in SOZ and non-SOZ electrodes during successful word encoding compared to nontask. Successful word encoding was associated with a reduction in local electrographic functional connectivity (increased REN), which was most exaggerated in temporal lobe SOZ. The IES rates were reduced during task, but only in the non-SOZ electrodes. Compared with nontask, REN features during task yielded marginal improvements in SOZ classification. SIGNIFICANCE: Previous studies have supported REN as a biomarker for epileptic brain. We show that REN differences between SOZ and non-SOZ are enhanced during a verbal memory task. We also show that IESs are reduced during task in non-SOZ, but not in SOZ. These findings support the hypothesis that SOZ and non-SOZ respond differently to task and warrant further exploration into the use of cognitive tasks to identify functioning memory circuits and localize SOZ.

Zobrazit více v PubMed

Lüders H, Najm I, Nair D, Widdess-Walsh P, Bingman W. The epileptogenic zone: General principles. Epileptic Disord. 2006. August/01;8 Suppl 2:S1–9. PubMed

Mohan M, Keller S, Nicolson A, Biswas S, Smith D, Osman Farah J, et al. The long-term outcomes of epilepsy surgery. PLoS One. 2018;13:e0196274. PubMed PMC

Engel J, Pedley TA, Aicardi J. Epilepsy: A Comprehensive Textbook: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2008.

Jehi L, Yardi R, Chagin K, Tassi L, Russo GL, Worrell G, et al. Development and validation of nomograms to provide individualised predictions of seizure outcomes after epilepsy surgery: a retrospective analysis. Lancet Neurol. 2015 2015/March/01/;14:283–290. PubMed

Van Gompel JJ, Worrell GA, Bell ML, Patrick TA, Cascino GD, Raffel C, et al. Intracranial electroencephalography with subdural grid electrodes: Techniques, complications, outcomes. Neurosurgery. 2008;63:498–506. PubMed

Téllez-Zenteno JF, Ronquillo LH, Moien-Afshari F, Wiebe S. Surgical outcomes in lesional and non-lesional epilepsy: A systematic review and meta-analysis. Epilepsy Res. 2010 2010/May/01/;89:310–318. PubMed

Avanzini G, Depaulis A, Tassinari A, de Curtis M. Do seizures and epileptic activity worsen epilepsy and deteriorate cognitive function? Epilepsia. 2013;54:14–21. PubMed

Brázdil M, Cimbálník J, Roman R, Shaw DJ, Stead MM, Daniel P, et al. Impact of cognitive stimulation on ripples within human epileptic and non-epileptic hippocampus. BMC Neurosci. 2015. July 25;16:47. PubMed PMC

Cimbalnik J, Pail M, Klimes P, Travnicek V, Roman R, Vajcner A, et al. Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy. Front Neurol. 2020;11:578571. PubMed PMC

Pail M, Cimbálník J, Roman R, Daniel P, Shaw DJ, Chrastina J, et al. High frequency oscillations in epileptic and non-epileptic human hippocampus during a cognitive task. Sci Rep. 2020. October 23;10:18147. PubMed PMC

Liu S, Parvizi J. Cognitive refractory state caused by spontaneous epileptic high-frequency oscillations in the human brain. Sci Transl Med. 2019;11:eaax7830. PubMed

Horak PC, Meisenhelter S, Song Y, Testorf ME, Kahana MJ, Viles WD, et al. Interictal epileptiform discharges impair word recall in multiple brain areas. Epilepsia. 2017;58:373–380. PubMed PMC

Ung H, Cazares C, Nanivadekar A, Kini L, Wagenaar J, Becker D, et al. Interictal epileptiform activity outside the seizure onset zone impacts cognition. Brain. 2017;140:2157–2168. PubMed PMC

Dauwels J, Eskandar E, Cash S, editors. Localization of seizure onset area from intracranial non-seizure EEG by exploiting locally enhanced synchrony. 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society; 2009 3-6 Sept. 2009. PubMed

Worrell G, Gotman J. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med. 2011;5:557–566. PubMed PMC

Varatharajah Y, Berry BM, Kalbarczyk ZT, Brinkmann BH, Worrell GA, Iyer RK, editors. Inter-ictal Seizure Onset Zone localization using unsupervised clustering and Bayesian Filtering. 2017 8th International IEEE/EMBS Conference on Neural Engineering (NER); 2017 25-28 May 2017.

Cimbalnik J, Brinkmann B, Kremen V, Jurak P, Berry B, Gompel JV, et al. Physiological and pathological high frequency oscillations in focal epilepsy. Ann Clin Transl Neurol. 2018;5:1062–1076. PubMed PMC

Jacobs J, Wu JY, Perucca P, Zelmann R, Mader M, Dubeau F, et al. Removing high-frequency oscillations: A prospective multicenter study on seizure outcome. Neurology. 2018;91:e1040–e1052. PubMed PMC

Cimbalnik J, Klimes P, Sladky V, Nejedly P, Jurak P, Pail M, et al. Multi-feature localization of epileptic foci from interictal, intracranial EEG. Clin Neurophysiol. 2019 2019/October/01/;130:1945–1953. PubMed PMC

Kleen JK, Scott RC, Holmes GL, Roberts DW, Rundle MM, Testorf M, et al. Hippocampal interictal epileptiform activity disrupts cognition in humans. Neurology. 2013;81:18–24. PubMed PMC

Shuman T, Amendolara B, Golshani P. Theta Rhythmopathy as a Cause of Cognitive Disability in TLE. Epilepsy Curr. 2017. Mar-Apr;17:107–111. PubMed PMC

Young JJ, Rudebeck PH, Marcuse LV, Fields MC, Yoo JY, Panov F, et al. Theta band network supporting human episodic memory is not activated in the seizure onset zone. Neuroimage. 2018 2018/December/01/;183:565–573. PubMed PMC

Warren CP, Hu S, Stead M, Brinkmann BH, Bower MR, Worrell GA. Synchrony in Normal and Focal Epileptic Brain: The Seizure Onset Zone is Functionally Disconnected. J Neurophysiol. 2010;104:3530–3539. PubMed PMC

Burns SP, Santaniello S, Yaffe RB, Jouny CC, Crone NE, Bergey GK, et al. Network dynamics of the brain and influence of the epileptic seizure onset zone. Proc Natl Acad Sci U S A. 2014;111:E5321–E5330. PubMed PMC

Varatharajah Y, Berry B, Cimbalnik J, Kremen V, Van Gompel J, Stead M, et al. Integrating artificial intelligence with real-time intracranial EEG monitoring to automate interictal identification of seizure onset zones in focal epilepsy. J Neural Eng. 2018;15:046035. PubMed PMC

Becker JT, Mintun MA, Diehl DJ, Dobkin J, Martidis A, Madoff DC, et al. Functional neuroanatomy of verbal free recall: A replication study. Hum Brain Mapp. 1994 1994/January/01;1:284–292. PubMed

Fischl B, van der Kouwe A, Destrieux C, Halgren E, Ségonne F, Salat DH, et al. Automatically Parcellating the Human Cerebral Cortex. Cereb Cortex. 2004;14:11–22. PubMed

Kucewicz MT, Berry BM, Kremen V, Brinkmann BH, Sperling MR, Jobst BC, et al. Dissecting gamma frequency activity during human memory processing. Brain. 2017;140:1337–1350. PubMed

Saboo KV, Varatharajah Y, Berry BM, Kremen V, Sperling MR, Davis KA, et al. Unsupervised machine-learning classification of electrophysiologically active electrodes during human cognitive task performance. Sci Rep. 2019 2019/November/22;9:17390. PubMed PMC

Kremen V, Duque JJ, Brinkmann BH, Berry BM, Kucewicz MT, Khadjevand F, et al. Behavioral State Classification in Epileptic Brain using Intracranial Electrophysiology. J Neural Eng. 2017. 01/04 03/29/nihms-submitted 04/01/pmc-release;14:026001–026001. PubMed PMC

Kremen V, Brinkmann BH, Van Gompel JJ, Stead M, St Louis EK, Worrell GA. Automated unsupervised behavioral state classification using intracranial electrophysiology. J Neural Eng. 2019 2019/January/21;16:026004. PubMed

Barkmeier DT, Shah AK, Flanagan D, Atkinson MD, Agarwal R, Fuerst DR, et al. High inter-reviewer variability of spike detection on intracranial EEG addressed by an automated multi-channel algorithm. Clin Neurophysiol. 2012;123:1088–1095. PubMed PMC

Kucewicz MT, Saboo K, Berry BM, Kremen V, Miller LR, Khadjevand F, et al. Human Verbal Memory Encoding Is Hierarchically Distributed in a Continuous Processing Stream. eNeuro. 2019;6:ENEURO.0214-0218.2018. PubMed PMC

Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR. Theta and Gamma Oscillations during Encoding Predict Subsequent Recall. J Neurosci. 2003;23:10809–10814. PubMed PMC

Fellner M-C, Gollwitzer S, Rampp S, Kreiselmeyr G, Bush D, Diehl B, et al. Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation. PLOS Biology. 2019;17:e3000403. PubMed PMC

Matsumoto JY, Stead M, Kucewicz MT, Matsumoto AJ, Peters PA, Brinkmann BH, et al. Network oscillations modulate interictal epileptiform spike rate during human memory. Brain. 2013;136:2444–2456. PubMed PMC

Kucewicz MT, Worrell GA, Gotman J. Pathologic brain network activity: memory impairment in epilepsy. Neurology 2013;81:12–13. PubMed PMC

Khambhati AN, Davis KA, Lucas TH, Litt B, Bassett DS. Virtual Cortical Resection Reveals Push-Pull Network Control Preceding Seizure Evolution. Neuron. 2016 2016/September/07/;91:1170–1182. PubMed PMC

Binder JR, Desai RH. The neurobiology of semantic memory. Trends Cogn Sci. 2011 2011/November/01/;15:527–536. PubMed PMC

Sanz-Garcia A, Rings T, Lehnertz K. Impact of type of intracranial EEG sensors on link strengths of evolving functional brain networks. Physiol Meas. 2018 2018/July/16;39:074003. PubMed

Youngerman BE, Khan FA, McKhann GM. Stereoelectroencephalography in epilepsy, cognitive neurophysiology, and psychiatric disease: safety, efficacy, and place in therapy. Neuropsychiatr Dis Treat. 2019;15:1701–1716. PubMed PMC

Quiroga RQ, Arnhold J, Lehnertz K, Grassberger P. Kulback-Leibler and renormalized entropies: Applications to electroencephalograms of epilepsy patients. Physical Review E. 2000. December/01/;62:8380–8386. PubMed

Murin Y, Kim J, Parvizi J, Goldsmith A. SozRank: A new approach for localizing the epileptic seizure onset zone. PLoS Comput Biol. 2018;14:e1005953. PubMed PMC

Varatharajah Y, Chong MJ, Saboo K, Berry BM, Brinkmann BH, Worrell GA, et al. EEG-GRAPH: A Factor-Graph-Based Model for Capturing Spatial, Temporal, and Observational Relationships in Electroencephalograms. NIPS 2017. Conference Procedings

Lin J-J, Rugg MD, Das S, Stein J, Rizzuto DS, Kahana MJ, et al. Theta band power increases in the posterior hippocampus predict successful episodic memory encoding in humans. Hippocampus. 2017;27:1040–1053. PubMed PMC

Brinkmann BH, Patterson EE, Vite C, Vasoli VM, Crepeau D, Stead M, et al. Forecasting Seizures Using Intracranial EEG Measures and SVM in Naturally Occurring Canine Epilepsy. PLoS One. 2015;10:e0133900. PubMed PMC

Park Y, Luo L, Parhi KK, Netoff T. Seizure prediction with spectral power of EEG using cost-sensitive support vector machines. Epilepsia. 2011;52:1761–1770. PubMed

Avoli M, Biagini G, de Curtis M. Do interictal spikes sustain seizures and epileptogenesis? Epilepsy Curr. 2006. Nov-Dec;6:203–207. PubMed PMC

Marsh ED, Peltzer B, Brown MW 3rd, Wusthoff C, Storm PB Jr., Litt B, et al. Interictal EEG spikes identify the region of electrographic seizure onset in some, but not all, pediatric epilepsy patients. Epilepsia. 2010;51:592–601. PubMed PMC

Goncharova II, Spencer SS, Duckrow RB, Hirsch LJ, Spencer DD, Zaveri HP. Intracranially recorded interictal spikes: Relation to seizure onset area and effect of medication and time of day. Clin Neurophysiol. 2013 2013/November/01/;124:2119–2128. PubMed

Hu S, Stead M, Dai Q, Worrell GA. On the Recording Reference Contribution to EEG Correlation, Phase Synchorony, and Coherence. IEEE Transactions on Systems, Man, and Cybernetics, Part B (Cybernetics). 2010;40:1294–1304. PubMed PMC

Ruis C Monitoring cognition during awake brain surgery in adults: A systematic review. J Clin Exp Neuropsychol. 2018 2018/November/26;40:1081–1104. PubMed

Vogt VL, Äikiä M, del Barrio A, Boon P, Borbély C, Bran E, et al. Current standards of neuropsychological assessment in epilepsy surgery centers across Europe. Epilepsia. 2017 2017/March/01;58:343–355. PubMed

Skrap M, Marin D, Ius T, Fabbro F, Tomasino B. Brain mapping: a novel intraoperative neuropsychological approach. J Neurosurg. 2016. October;125:877–887. PubMed

Shomstein S Cognitive functions of the posterior parietal cortex: top-down and bottom-up attentional control. Front Integr Neurosci. 2012 2012-July-04;6. Mini Review PubMed PMC

Brownsett SLE, Wise RJS. The Contribution of the Parietal Lobes to Speaking and Writing. Cereb Cortex. 2010;20:517–523. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...