Download PDF
CC BY 4.0 · Arq Neuropsiquiatr 2023; 81(05): 492-501
DOI: 10.1055/s-0043-1761493
View and Review

Rhinal and hippocampal event-related potentials as epileptogenic zone markers in the pre-surgical evaluation of temporal epilepsies: a systematic review

Potenciais evocados rinais e hipocampais como marcadores da zona epileptogênica na avaliação pré-cirúrgica das epilepsias temporais: uma revisão sistemática
Daniela de Andrade Morange 
1   Institut de Neurosciences des Systèmes, Université d'Aix-Marseille, Marseille, France.
2   Hospital Universitário Prof. Edgard Santos, Departamento de Neurofisiologia Clínica, Salvador BA, Brazil.
,
Magali Teresópolis Reis Amaral 
3   Universidade Estadual de Feira de Santana, Departamento de Ciências Exatas, Salvador BA, Brazil.
,
Martha Silvia Martinez-Silveira 
4   Fundação Oswaldo Cruz, Instituto Gonçalo Muniz, Salvador BA, Brazil.
,
Agnès Trébuchon 
1   Institut de Neurosciences des Systèmes, Université d'Aix-Marseille, Marseille, France.
5   Neurophysiologie Clinique, Assistance Publique - Hôpitaux de Marseille, Hôpital de la Timone, Marseille, France.
› Author Affiliations
› Further Information
Also available at
   Permissions and Reprints

Abstract

Background Cognitive event-related potentials (ERPs) allow for lateralization of the epileptogenic zone (EZ) to estimate the reserve of memory in the contralateral non-epileptogenic hemisphere, and to investigate the prognosis of temporal lobe seizure control in unilateral temporal lobe epilepsy (TLE).

Objective To define the accuracy of cognitive evoked anterior mesial temporal lobe (AMTL-N400) and P600 potentials in detecting the epileptogenic zone in temporal lobe epilepsy (TLE), and second, to evaluate the possibility of using them as markers of cognitive outcome.

Methods The systematic review using Medline/PubMed, Embase, and Lilacs database was conducted in September 2021. Only articles published in English from 1985 to June 2021 were included. We searched for studies with: (1) depth intracranial electroencephalography (iEEG) recordings analysis of rhinal and hippocampal activity (2) correlations between ERP results obtained in the mesial temporal regions (AMTL-N400 and P600) and the epileptogenic zone.

Results Six out of the seven studies included in this review defined the laterality of the epileptogenic zone (EZ) during presurgical investigation using ERPs. One study showed that the contralateral AMTL-N400 predicts seizure control. Another study found correlation between the amplitudes of the right AMTL-N400 and postoperative memory performance.

Conclusions There is evidence that the reduced amplitude of the AMTL-N400 has high accuracy in identifying the epileptogenic zone, as it does in estimating the extent of seizure control and memory impairment in postoperative patients.

Resumo

Antecedentes Potenciais relacionados a eventos (PREs) cognitivos permitem a lateralização da zona epileptogênica (ZE), estimar a reserva de memória no hemisfério contralateral não-epileptogênico, e estimar o prognóstico pós-operatório em pacientes com epilepsia do lobo temporal (ELT) unilateral quanto ao controle de crises.

Objetivo Definir a acurácia dos potenciais evocados cognitivos do lobo temporal mesial anterior (LTMA-N400) e P600 na detecção da zona epileptogênica na epilepsia do lobo temporal (ELT), além de avaliar a possibilidade de usá-los como marcadores de desfecho cognitivo.

Métodos A revisão sistemática foi realizada em setembro de 2021 usando as bases de dados Medline/PubMed, Embase e Lilacs. Apenas artigos publicados em inglês no período entre 1985 e junho de 2021 foram incluídos. Buscamos estudos com: (1) análises dos registros de electroencefalografia intracraniana (EEGi) da atividade rinal e hipocampal (2) correlações entre os resultados de PREs obtidos nas regiões temporais mesiais (AMTL-N400 e P600) e a zona epileptogênica.

Resultados Seis dos sete estudos incluídos nesta revisão definiram a lateralidade da zona epileptogênica (ZE) durante a investigação pré-cirúrgica usando PREs. Um estudo mostrou que o AMTL-N400 contralateral prediz o controle das crises. Outro estudo encontrou correlação entre as amplitudes do AMTL-N400 direito e o desempenho da memória pós-operatória.

Conclusões Há evidências de que a amplitude reduzida do AMTL-N400 tem alta precisão na identificação da zona epileptogênica, assim como na estimativa do prognóstico quanto ao controle de crises a longo prazo e prejuízo da memória em pacientes submetidos à cirurgia ressectiva.

Keywords

Evoked Potentials - Epilepsy - Temporal Lobe - Memory - Perirhinal Cortex - Hippocampus

Palavras-chave

Potenciais Evocados - Epilepsia do Lobo Temporal - Memória - Córtex Perirrinal - Hipocampo

Authors' Contributions

DAM: conceptualization, data curation, statistical analysis, writing-original draft, and methodology; MSMS: methodology, search strategies, database searches, writing-review & editing; AT: data curation, writing-review & editing; MTRA: methodology, statistical analysis, and results. All authors read, discussed, and approved the final manuscript.




Publication History

Received: 14 December 2021

Accepted: 20 August 2022

Article published online:
31 May 2023

© 2023. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution 4.0 International License, permitting copying and reproduction so long as the original work is given appropriate credit (https://creativecommons.org/licenses/by/4.0/)

Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil

 

  • References

  • 1 McCarthy G, Nobre AC, Bentin S, Spencer DD. Language-related field potentials in the anterior-medial temporal lobe: I. Intracranial distribution and neural generators. J Neurosci 1995; 15 (02) 1080-1089
    CrossrefPubMedSearch in Google Scholar
  • 2 Barbeau EJ, Chauvel P, Moulin CJ, Regis J, Liégeois-Chauvel C. Hippocampus duality: Memory and novelty detection are subserved by distinct mechanisms. Hippocampus 2017; 27 (04) 405-416
    CrossrefPubMedSearch in Google Scholar
  • 3 Balter S, Lin G, Leyden KM, Paul BM, McDonald CR. Neuroimaging correlates of language network impairment and reorganization in temporal lobe epilepsy. Brain Lang 2019; 193: 31-44
    CrossrefPubMedSearch in Google Scholar
  • 4 Squire LR, Stark CE, Clark RE. The medial temporal lobe. Annu Rev Neurosci 2004; 27: 279-306
    CrossrefPubMedSearch in Google Scholar
  • 5 Baxendale S, Thompson P. Red flags in epilepsy surgery: Identifying the patients who pay a high cognitive price for an unsuccessful surgical outcome. Epilepsy Behav 2018; 78: 269-272
    CrossrefPubMedSearch in Google Scholar
  • 6 Grunwald T, Kurthen M. Novelty detection and encoding for declarative memory within the human hippocampus. Clin EEG Neurosci 2006; 37 (04) 309-314
    CrossrefPubMedSearch in Google Scholar
  • 7 Elger CE, Grunwald T, Lehnertz K. et al. Human temporal lobe potentials in verbal learning and memory processes. Neuropsychologia 1997; 35 (05) 657-667
    CrossrefPubMedSearch in Google Scholar
  • 8 Grunwald T, Elger CE, Lehnertz K, Van Roost D, Heinze HJ. Alterations of intrahippocampal cognitive potentials in temporal lobe epilepsy. Electroencephalogr Clin Neurophysiol 1995; 95 (01) 53-62
    CrossrefPubMedSearch in Google Scholar
  • 9 Grunwald T, Lehnertz K, Heinze HJ, Helmstaedter C, Elger CE. Verbal novelty detection within the human hippocampus proper. Proc Natl Acad Sci U S A 1998; 95 (06) 3193-3197
    CrossrefPubMedSearch in Google Scholar
  • 10 Grunwald T, Lehnertz K, Pezer N. et al. Prediction of postoperative seizure control by hippocampal event-related potentials. Epilepsia 1999; 40 (03) 303-306
    CrossrefPubMedSearch in Google Scholar
  • 11 Smith ME, Stapleton JM, Halgren E. Human medial temporal lobe potentials evoked in memory and language tasks. Electroencephalogr Clin Neurophysiol 1986; 63 (02) 145-159
    CrossrefPubMedSearch in Google Scholar
  • 12 Chelune GJ. Hippocampal adequacy versus functional reserve: predicting memory functions following temporal lobectomy. Arch Clin Neuropsychol 1995; 10 (05) 413-432
    CrossrefPubMedSearch in Google Scholar
  • 13 Ono SE, Mader-Joaquim MJ, de Carvalho Neto A, de Paola L, Dos Santos GR, Silvado CES. Relationship between hippocampal subfields and Verbal and Visual memory function in Mesial Temporal Lobe Epilepsy patients. Epilepsy Res 2021; 175: 106700
    CrossrefPubMedSearch in Google Scholar
  • 14 Rodrigues GR, Kandratavicius L, Peixoto-Santos JE. et al. Increased frequency of hippocampal sclerosis ILAE type 2 in patients with mesial temporal lobe epilepsy with normal episodic memory. Brain 2015; 138 (Pt 6): e359
    CrossrefPubMedSearch in Google Scholar
  • 15 Witt JA, Coras R, Schramm J. et al. The overall pathological status of the left hippocampus determines preoperative verbal memory performance in left mesial temporal lobe epilepsy. Hippocampus 2014; 24 (04) 446-454
    CrossrefPubMedSearch in Google Scholar
  • 16 Halgren E, Squires NK, Wilson CL, Rohrbaugh JW, Babb TL, Crandall PH. Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events. Science 1980; 210 (4471): 803-805
    CrossrefPubMedSearch in Google Scholar
  • 17 Kneebone AC, Chelune GJ, Dinner DS, Naugle RI, Awad IA. Intracarotid amobarbital procedure as a predictor of material-specific memory change after anterior temporal lobectomy. Epilepsia 1995; 36 (09) 857-865
    CrossrefPubMedSearch in Google Scholar
  • 18 Baxendale S. Neuropsychological assessment in epilepsy. Pract Neurol 2018; 18 (01) 43-48
    CrossrefPubMedSearch in Google Scholar
  • 19 Shamseer L, Moher D, Clarke M. et al; PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 2015; 350: g7647
    CrossrefPubMedSearch in Google Scholar
  • 20 Moola S, Munn Z, Tufanaru C. et al. Systematic reviews of etiology and risk. Appendix 7.5 Critical appraisal checklist for analytical cross-sectional studies. In: Aromataris E, Z M, editors. JBI Manual for Evidence Synthesis: JBI; 2020. Available from: https://synthesismanual.jbi.global
    Crossref
  • 21 Guillem F, N'Kaoua B, Rougier A, Claverie B. Intracranial topography of event-related potentials (N400/P600) elicited during a continuous recognition memory task. Psychophysiology 1995; 32 (04) 382-392
    CrossrefPubMedSearch in Google Scholar
  • 22 Guillem F, N'Kaoua B, Rougier A, Claverie B. Location of the epileptic zone and its physiopathological effects on memory-related activity of the temporal lobe structures: a study with intracranial event-related potentials. Epilepsia 1998; 39 (09) 928-941
    CrossrefPubMedSearch in Google Scholar
  • 23 Fernández G, Effern A, Grunwald T. et al. Real-time tracking of memory formation in the human rhinal cortex and hippocampus. Science 1999; 285 (5433): 1582-1585
    CrossrefPubMedSearch in Google Scholar
  • 24 Dietl T, Kurthen M, Kirch D. et al. Limbic event-related potentials to words and pictures in the presurgical evaluation of temporal lobe epilepsy. Epilepsy Res 2008; 78 (2-3): 207-215
    CrossrefPubMedSearch in Google Scholar
  • 25 Grunwald T, Lehnertz K, Helmstaedter C. et al. Limbic ERPs predict verbal memory after left-sided hippocampectomy. Neuroreport 1998; 9 (15) 3375-3378
    CrossrefPubMedSearch in Google Scholar
  • 26 Mormann F, Fernández G, Klaver P, Weber B, Elger CE, Fell J. Declarative memory formation in hippocampal sclerosis: an intracranial event-related potentials study. Neuroreport 2007; 18 (04) 317-321
    CrossrefPubMedSearch in Google Scholar
  • 27 Puce A, Andrewes DG, Berkovic SF, Bladin PF. Visual recognition memory. Neurophysiological evidence for the role of temporal white matter in man. Brain 1991; 114 (Pt 4): 1647-1666
    CrossrefPubMedSearch in Google Scholar