Electrophysiological Biomarkers of Epileptogenicity in Alzheimer's Disease

Overview

Journal Front Hum Neurosci

Specialty Neurology

Date 2021 Dec 17

PMID 34916917

Citations 11

Authors

Tingting Yu

Xiao Liu

Jianping Wu

Qun Wang

Affiliations

Soon will be listed here.

Abstract

Cortical network hyperexcitability is an inextricable feature of Alzheimer's disease (AD) that also might accelerate its progression. Seizures are reported in 10-22% of patients with AD, and subclinical epileptiform abnormalities have been identified in 21-42% of patients with AD without seizures. Accurate identification of hyperexcitability and appropriate intervention to slow the compromise of cognitive functions of AD might open up a new approach to treatment. Based on the results of several studies, epileptiform discharges, especially those with specific features (including high frequency, robust morphology, right temporal location, and occurrence during awake or rapid eye movement states), frequent small sharp spikes (SSSs), temporal intermittent rhythmic delta activities (TIRDAs), and paroxysmal slow wave events (PSWEs) recorded in long-term scalp electroencephalogram (EEG) provide sufficient sensitivity and specificity in detecting cortical network hyperexcitability and epileptogenicity of AD. In addition, magnetoencephalogram (MEG), foramen ovale (FO) electrodes, and computational approaches help to find subclinical seizures that are invisible on scalp EEGs. We performed a comprehensive analysis of the aforementioned electrophysiological biomarkers of AD-related seizures.

Citing Articles

Functional network disruption in cognitively unimpaired autosomal dominant Alzheimer's disease: a magnetoencephalography study.

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Alzheimer's Disease and Epilepsy: Exploring Shared Pathways and Promising Biomarkers for Future Treatments.

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Local signal variability and functional connectivity: Sensitive measures of the excitation-inhibition ratio?.

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McArdle C, Arnone A, Heaney C, Raab-Graham K Front Psychiatry. 2024; 14:1296527.

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Network Hyperexcitability in Early Alzheimer's Disease: Is Functional Connectivity a Potential Biomarker?.

Stam C, van Nifterick A, de Haan W, Gouw A Brain Topogr. 2023; 36(4):595-612.

PMID: 37173584 PMC: 10293463. DOI: 10.1007/s10548-023-00968-7.

References

Sperling M, Mendius J, Engel Jr J . Mesial temporal spikes: a simultaneous comparison of sphenoidal, nasopharyngeal, and ear electrodes. Epilepsia. 1986; 27(1):81-6. DOI: 10.1111/j.1528-1157.1986.tb03505.x. View

Palop J, Mucke L . Epilepsy and cognitive impairments in Alzheimer disease. Arch Neurol. 2009; 66(4):435-40. PMC: 2812914. DOI: 10.1001/archneurol.2009.15. View

Tyvaert L, Levan P, Dubeau F, Gotman J . Noninvasive dynamic imaging of seizures in epileptic patients. Hum Brain Mapp. 2009; 30(12):3993-4011. PMC: 3767605. DOI: 10.1002/hbm.20824. View

Lam A, Cole A, Cash S . New Approaches to Studying Silent Mesial Temporal Lobe Seizures in Alzheimer's Disease. Front Neurol. 2019; 10:959. PMC: 6737997. DOI: 10.3389/fneur.2019.00959. View

Koessler L, Cecchin T, Colnat-Coulbois S, Vignal J, Jonas J, Vespignani H . Catching the invisible: mesial temporal source contribution to simultaneous EEG and SEEG recordings. Brain Topogr. 2014; 28(1):5-20. DOI: 10.1007/s10548-014-0417-z. View

Naftulin J, Ahmed O, Piantoni G, Eichenlaub J, Martinet L, Kramer M . Ictal and preictal power changes outside of the seizure focus correlate with seizure generalization. Epilepsia. 2018; 59(7):1398-1409. PMC: 6031475. DOI: 10.1111/epi.14449. View

Lam A, Deck G, Goldman A, Eskandar E, Noebels J, Cole A . Silent hippocampal seizures and spikes identified by foramen ovale electrodes in Alzheimer's disease. Nat Med. 2017; 23(6):678-680. PMC: 5461182. DOI: 10.1038/nm.4330. View

Zott B, Busche M, Sperling R, Konnerth A . What Happens with the Circuit in Alzheimer's Disease in Mice and Humans?. Annu Rev Neurosci. 2018; 41:277-297. PMC: 6571139. DOI: 10.1146/annurev-neuro-080317-061725. View

Brown R, Lam A, Gonzalez-Sulser A, Ying A, Jones M, Chou R . Circadian and Brain State Modulation of Network Hyperexcitability in Alzheimer's Disease. eNeuro. 2018; 5(2). PMC: 5956746. DOI: 10.1523/ENEURO.0426-17.2018. View

10.

Yang C, Zhong S, Zhou X, Wei L, Wang L, Nie S . The Abnormality of Topological Asymmetry between Hemispheric Brain White Matter Networks in Alzheimer's Disease and Mild Cognitive Impairment. Front Aging Neurosci. 2017; 9:261. PMC: 5545578. DOI: 10.3389/fnagi.2017.00261. View

11.

Bakker A, Krauss G, Albert M, Speck C, Jones L, Stark C . Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron. 2012; 74(3):467-74. PMC: 3351697. DOI: 10.1016/j.neuron.2012.03.023. View

12.

Kam K, Duffy A, Moretto J, LaFrancois J, Scharfman H . Interictal spikes during sleep are an early defect in the Tg2576 mouse model of β-amyloid neuropathology. Sci Rep. 2016; 6:20119. PMC: 4730189. DOI: 10.1038/srep20119. View

13.

Malow B, Kushwaha R, Lin X, Morton K, Aldrich M . Relationship of interictal epileptiform discharges to sleep depth in partial epilepsy. Electroencephalogr Clin Neurophysiol. 1997; 102(1):20-6. DOI: 10.1016/s0013-4694(96)96028-9. View

14.

Milikovsky D, Ofer J, Senatorov Jr V, Friedman A, Prager O, Sheintuch L . Paroxysmal slow cortical activity in Alzheimer's disease and epilepsy is associated with blood-brain barrier dysfunction. Sci Transl Med. 2019; 11(521). DOI: 10.1126/scitranslmed.aaw8954. View

15.

Lam A, Sarkis R, Pellerin K, Jing J, Dworetzky B, Hoch D . Association of epileptiform abnormalities and seizures in Alzheimer disease. Neurology. 2020; 95(16):e2259-e2270. PMC: 7713786. DOI: 10.1212/WNL.0000000000010612. View

16.

Busche M, Konnerth A . Neuronal hyperactivity--A key defect in Alzheimer's disease?. Bioessays. 2015; 37(6):624-32. DOI: 10.1002/bies.201500004. View

17.

Wennberg R, Valiante T, Cheyne D . EEG and MEG in mesial temporal lobe epilepsy: where do the spikes really come from?. Clin Neurophysiol. 2011; 122(7):1295-313. DOI: 10.1016/j.clinph.2010.11.019. View

18.

Normand M, Wszolek Z, KLASS D . Temporal intermittent rhythmic delta activity in electroencephalograms. J Clin Neurophysiol. 1995; 12(3):280-4. DOI: 10.1097/00004691-199505010-00005. View

19.

Noachtar S, Remi J . The role of EEG in epilepsy: a critical review. Epilepsy Behav. 2009; 15(1):22-33. DOI: 10.1016/j.yebeh.2009.02.035. View

20.

Musaeus C, Engedal K, Hogh P, Jelic V, Morup M, Naik M . EEG Theta Power Is an Early Marker of Cognitive Decline in Dementia due to Alzheimer's Disease. J Alzheimers Dis. 2018; 64(4):1359-1371. DOI: 10.3233/JAD-180300. View