Advertisement

Brain Topography

, Volume 28, Issue 1, pp 5–20 | Cite as

Catching the Invisible: Mesial Temporal Source Contribution to Simultaneous EEG and SEEG Recordings

  • Laurent Koessler
  • Thierry Cecchin
  • Sophie Colnat-Coulbois
  • Jean-Pierre Vignal
  • Jacques Jonas
  • Hervé Vespignani
  • Georgia Ramantani
  • Louis Georges Maillard
Original Paper

Abstract

Mesial temporal sources are presumed to escape detection in scalp electroencephalographic recordings. This is attributed to the deep localization and infolded geometry of mesial temporal structures that leads to a cancellation of electrical potentials, and to the blurring effect of the superimposed neocortical background activity. In this study, we analyzed simultaneous scalp and intracerebral electroencephalographic recordings to delineate the contribution of mesial temporal sources to scalp electroencephalogram. Interictal intracerebral spike networks were classified in three distinct categories: solely mesial, mesial as well as neocortical, and solely neocortical. The highest and earliest intracerebral spikes generated by the leader source of each network were marked and the corresponding simultaneous intracerebral and scalp electroencephalograms were averaged and then characterized both in terms of amplitude and spatial distribution. In seven drug-resistant epileptic patients, 21 interictal intracerebral networks were identified: nine mesial, five mesial plus neocortical and seven neocortical. Averaged scalp spikes arising respectively from mesial, mesial plus neocortical and neocortical networks had a 7.1 (n = 1,949), 36.1 (n = 628) and 10 (n = 1,471) µV average amplitude. Their scalp electroencephalogram electrical field presented a negativity in the ipsilateral anterior and basal temporal electrodes in all networks and a significant positivity in the fronto-centro-parietal electrodes solely in the mesial plus neocortical and neocortical networks. Topographic consistency test proved the consistency of these different scalp electroencephalogram maps and hierarchical clustering clearly differentiated them. In our study, we have thus shown for the first time that mesial temporal sources (1) cannot be spontaneously visible (mean signal-to-noise ratio −2.1 dB) on the scalp at the single trial level and (2) contribute to scalp electroencephalogram despite their curved geometry and deep localization.

Keywords

Simultaneous EEG–SEEG recordings Deep brain sources Source localization Mesial temporal lobe epilepsy Hippocampus Volume conduction 

Abbreviations

IIS

Interictal intracerebral spikes

ISS

Interictal scalp spikes

M

Mesial epileptic network

NC

Neocortical epileptic network

M + NC

Mesial and neocortical epileptic network

MTL

Mesial temporal lobe

SEEG

Stereoelectroencephalography

Notes

Acknowledgments

The Authors would like to thank Cécile Popko (Université de Lorraine) for EEG-SEEG data management. This study was supported by the French Ministry of Health (PHRC 17-05, 2009) and the Regional Council of Lorraine.

Supplementary material

10548_2014_417_MOESM1_ESM.tif (2.8 mb)
Supplementary material 1 (A) Averaged EEG signal and (B) 3D amplitude maps for the three spike networks in patient 1. The stars on the left of the electrode labels indicate that the corresponding averaged EEG signals at t 0 were statistically significant (Walsh’s test) (TIFF 2850 kb)
10548_2014_417_MOESM2_ESM.tif (1.5 mb)
Supplementary material 2 (A) Averaged EEG signal and (B) 3D amplitude maps for the two spike networks in patient 2. The stars on the left of the electrode labels indicate that the corresponding averaged EEG signals at t 0 were statistically significant (Walsh’s test) (TIFF 1532 kb)
10548_2014_417_MOESM3_ESM.tif (2 mb)
Supplementary material 3 (A) Averaged EEG signal and (B) 3D amplitude maps for the three spike networks in patient 3. The stars on the left of the electrode labels indicate that the corresponding averaged EEG signals at t 0 were statistically significant (Walsh’s test) (TIFF 2024 kb)
10548_2014_417_MOESM4_ESM.tif (1.5 mb)
Supplementary material 4 (A) Averaged EEG signal and (B) 3D amplitude maps for the two spike networks in patient 4. The stars on the left of the electrode labels indicate that the corresponding averaged EEG signals at t 0 were statistically significant (Walsh’s test) (TIFF 1516 kb)
10548_2014_417_MOESM5_ESM.tif (2.1 mb)
Supplementary material 5 (A) Averaged EEG signal and (B) 3D amplitude maps for the four spike networks in patient 6. The stars on the left of the electrode labels indicate that the corresponding averaged EEG signals at t 0 were statistically significant (Walsh’s test) (TIFF 2182 kb)
10548_2014_417_MOESM6_ESM.tif (2.3 mb)
Supplementary material 6 (A) Averaged EEG signal and (B) 3D amplitude maps for the four spike networks in patient 7. The stars on the left of the electrode labels indicate that the corresponding averaged EEG signals at t 0 were statistically significant (Walsh’s test). (TIFF 2309 kb)

References

  1. Abraham K, Ajmone-Marsan CA (1958) Patterns of cortical discharges and their relation to routine scalp electroencephalography. Electroencephalogr Clin Neurophysiol 10:447–461PubMedCrossRefGoogle Scholar
  2. Alarcon G, Guy CN, Binnie CD, Walker SR, Elwes RD, Polkey CE (1994) Intracerebral propagation of interictal activity in partial activity: implications for source localisation. J Neurol Neurosurg Psychiatry 57:435–449PubMedCentralPubMedCrossRefGoogle Scholar
  3. Alarcon G, Garcia Seoane JJ, Binnie CD, Martin Miguel MC, Juler J, Polkey CE et al (1997) Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. Brain 120:2259–2282PubMedCrossRefGoogle Scholar
  4. Barba C, Barbati G, Minotti L, Hoffmann D, Kahane P (2007) Ictal clinical and scalp-EEG findings differentiating temporal lobe epilepsies from temporal ‘plus’ epilepsies. Brain 130:1957–1967PubMedCrossRefGoogle Scholar
  5. Bartolomei F, Wendling F, Bellanger JJ, Régis J, Chauvel P (2001) Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin Neurophysiol 112:1746–1760PubMedCrossRefGoogle Scholar
  6. Bartolomei F, Chauvel P, Wendling F (2008) Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 131:1818–1830PubMedCrossRefGoogle Scholar
  7. Baumgartner C, Lindinger G, Ebner A, Aull S, Serles W, Olbrich A et al (1995) Propagation of interictal epileptic activity in temporal lobe epilepsy. Neurology 45:118–122PubMedCrossRefGoogle Scholar
  8. Bettus G, Wendling F, Guye M, Valton L, Régis J, Chauvel P, Bartolomei F (2008) Enhanced EEG functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res 81:58–68PubMedCrossRefGoogle Scholar
  9. Bragin A, Wilson CL, Engel J Jr (2000) Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia 41(Suppl 6):S144–S152PubMedCrossRefGoogle Scholar
  10. Chang BS, Schomer D, Niedermeyer E (2011a) Epilepsy in adults and the elderly. In: Schomer D, Lopes da Silva F (eds) Niedermeyer’s electroencephalography: basic principles, clinical applications, and related fields, MD: Wolters-Kluwer Lippincott Williams Wilkins, Baltimore, p 541–562Google Scholar
  11. Chang BS, Schomer D, Niedermeyer E (2011b) Normal EEG and sleep: adults and elderly. In: Schomer D, Lopes da Silva F (eds) Niedermeyer’s electroencephalography: basic principles, clinical applications, and related fields. MD: Wolters-Kluwer Lippincott Williams & Wilkins, Baltimore, p 183–214Google Scholar
  12. Chassoux F, Semah F, Bouilleret V, Landre E, Devaux B, Turak B et al (2004) Metabolic changes and electro-clinical patterns in mesio-temporal lobe epilepsy: a correlative study. Brain 127:164–174PubMedCrossRefGoogle Scholar
  13. Ebersole JS (2000) Sublobar localization of temporal neocortical epileptogenic foci by source modeling. Adv Neurol 84:353–363PubMedGoogle Scholar
  14. Ebersole JS, Wade PB (1991) Spike voltage topography identifies two types of fronto-temporal epileptic foci. Neurology 41:1425–1431PubMedCrossRefGoogle Scholar
  15. Eisenschenk S, Gilmore RL, Cibula JE, Roper SN (2001) Lateralization of temporal lobe foci: depth versus subdural electrodes. Clin Neurophysiol 112:836–844PubMedCrossRefGoogle Scholar
  16. Gavaret M, Badier JM, Marquis P, Bartolomei F, Chauvel P (2004) Electric source imaging in temporal lobe epilepsy. J Clin Neurophysiol 21:267–282PubMedCrossRefGoogle Scholar
  17. Gil-Nagel A, Risinger MW (1997) Ictal semiology in hippocampal versus extra hippocampal temporal lobe epilepsy. Brain 120:183–192PubMedCrossRefGoogle Scholar
  18. Grouiller F, Thornton RC, Groening K, Spinelli L, Duncan JS, Schaller K et al (2011) With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. Brain 134:2867–2886PubMedCentralPubMedCrossRefGoogle Scholar
  19. Harroud A, Bouthillier A, Weil AG, Nguyen DK (2012) Temporal lobe epilepsy surgery failures: a review. Epilepsy Res Treat 2012:201651PubMedCentralPubMedGoogle Scholar
  20. Homan RW, Jones MC, Tawat S (1988) Anterior temporal electrodes in complex partial seizures. Electroencephalogr Clin Neurophysiol 70:105–109PubMedCrossRefGoogle Scholar
  21. Jayakar P, Duchowny M, Resnick TJ, Alvarez LA (1991) Localization of seizure foci: pitfalls and caveats. J Clin Neurophysiol 8:414–431PubMedCrossRefGoogle Scholar
  22. Jonas J, Descoins M, Koessler L, Colnat-Coulbois S, Sauvée M, Guye M et al (2012) Focal electrical intracerebral stimulation of a face-sensitive area causes transient prosopagnosia. Neuroscience 222:281–288PubMedCrossRefGoogle Scholar
  23. Kahane P, Landré E, Minotti L, Francione S, Ryvlin P (2006) The Bancaud and Talairach view on the epileptogenic zone: a working hypothesis. Epileptic Disord 8:S16–S26PubMedGoogle Scholar
  24. Koenig T, Melie-García L (2010) A method to determine the presence of averaged event-related fields using randomization tests. Brain Topogr 23:233–242PubMedCrossRefGoogle Scholar
  25. Koessler L, Maillard L, Benhadid A, Vignal JP, Felblinger J, Vespignani H et al (2009) Automated cortical projection of EEG sensors: anatomical correlation via the international 10-10 system. Neuroimage 46:64–72PubMedCrossRefGoogle Scholar
  26. Koessler L, Benar C, Maillard L, Badier JM, Vignal JP, Bartolomei F et al (2010) Source localization of ictal epileptic activity investigated by high resolution EEG and validated by SEEG. Neuroimage 51:642–653PubMedCrossRefGoogle Scholar
  27. Lantz G, Holub M, Ryding E, Rosén I (1996) Simultaneous intracranial and extracranial recording of interictal epileptiform activity in patients with drug resistant partial epilepsy: patterns of conduction and results from dipole reconstructions. Electroencephalogr Clin Neurophysiol 99:69–78PubMedCrossRefGoogle Scholar
  28. Lantz G, Grave de Peralta R, Spinelli L, Seeck M, Michel CM (2003) Epileptic source localization with high density EEG: how many electrodes are needed? Clin Neurophysiol 114:63–69PubMedCrossRefGoogle Scholar
  29. Lieb JP, Walsh GO, Babb TL, Walter RD, Crandall PH (1976) A comparison of EEG seizure patterns recorded with surface and depth electrodes in patients with temporal lobe epilepsy. Epilepsia 17:137–160PubMedCrossRefGoogle Scholar
  30. Lopes da Silva, Van Rotterdam A (1993) Biophysical aspects of EEG and magnetoencephalogram generation. In: Niedermeyer E, Lopes da Silva F (edn) Electroencephalography: basic principles, clinical applications, and related fields. MD: Williams and Wilkins, Baltimore, p 93–109Google Scholar
  31. Maillard L, Vignal JP, Gavaret M, Guye M, Biraben A, McGonigal A et al (2004) Semiologic and electrophysiologic correlations in temporal lobe seizure subtypes. Epilepsia 45:1590–1599PubMedCrossRefGoogle Scholar
  32. Maillard L, Koessler L, Colnat-Coulbois S, Vignal JP, Louis-Dorr V, Marie PY (2009) Combined SEEG and source localization study of temporal lobe schizencephaly and polymicrogyria. Clin Neurophysiol 120:1628–1636PubMedCrossRefGoogle Scholar
  33. Maillard L, Barbeau EJ, Baumann C, Koessler L, Benar C, Chauvel P et al (2011) From perception to recognition memory: time course and lateralization of neural substrates of word and abstract picture processing. J Cogn Neurosci 23:782–800PubMedCrossRefGoogle Scholar
  34. Merlet I, Gotman J (1999) Reliability of dipole models of epileptic spikes. Clin Neurophysiol 110:1013–1028PubMedCrossRefGoogle Scholar
  35. Merlet I, Garcia-Larrea L, Ryvlin P, Isnard J, Sindou M, Mauguiere F (1998) Topographical reliability of mesio-temporal sources of interictal spikes in temporal lobe epilepsy. Electroencephalogr Clin Neurophysiol 107:206–212PubMedCrossRefGoogle Scholar
  36. Mikuni N, Nagamine T, Ikeda A, Terada K, Taki W, Kimura J et al (1997) Simultaneous recording of epileptiform discharges by MEG and subdural electrodes in temporal lobe epilepsy. Neuroimage 5:298–306PubMedCrossRefGoogle Scholar
  37. Nayak D, Valentín A, Alarcón G, García Seoane JJ, Brunnhuber F, Juler J et al (2004) Characteristics of scalp electrical fields associated with deep medial temporal epileptiform discharges. Clin Neurophysiol 115(6):1423–1435PubMedCrossRefGoogle Scholar
  38. Ramantani G, Koessler L, Colnat-Coulbois S, Vignal JP, Isnard J, Catenoix H et al (2013) Intracranial evaluation of the epileptogenic zone in regional infrasylvian polymicrogyria. Epilepsia 54:296–304PubMedCrossRefGoogle Scholar
  39. Sedat J, Duvernoy H (1990) Anatomical study of the temporal lobe. Correlations with nuclear magnetic resonance. J Neuroradiol 17:26–49PubMedGoogle Scholar
  40. Spencer S, Spencer D (1994) Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia 35:721–727PubMedCrossRefGoogle Scholar
  41. Van ‘t Ent D, Manshanden I, Ossenblok P, Velis DN, Verbunt JP et al (2003) Spike cluster analysis in neocortical localization related epilepsy yields clinically significant equivalent source localization results in magnetoencephalogram (MEG). Clin Neurophysiol 114(10):1948–1962PubMedCrossRefGoogle Scholar
  42. Walsh JE (1959) Large sample nonparametric rejection of outlying observations. Ann Inst Stat Math 10:223–232CrossRefGoogle Scholar
  43. Wennberg R, Cheyne D (2014) EEG source imaging of anterior temporal lobe spikes: validity and reliability. Clin Neurophysiol 125(5):886–902PubMedCrossRefGoogle Scholar
  44. Wieser HG (2004) ILAE Commission on Neurosurgery of Epilepsy. ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45:695–714PubMedCrossRefGoogle Scholar
  45. Wieser HG, Elger CE, Stodieck SR (1985) The ‘foramen ovale electrode’: a new recording method for the preoperative evaluation of patients suffering from mesio-basal temporal lobe epilepsy. Electroencephalogr Clin Neurophysiol 61:314–322PubMedCrossRefGoogle Scholar
  46. Williamson PD, Thadani VM, French JA, Darcey TM, Mattson RH, Spencer SS et al (1998) Medial temporal lobe epilepsy: videotape analysis of objective clinical seizure characteristics. Epilepsia 39:1182–1188PubMedCrossRefGoogle Scholar
  47. Yamazaki M, Tucker DM, Fujimoto A, Yamazoe T, Okanishi T, Yokota T, Enoki H, Yamamoto T (2012) Comparison of dense array EEG with simultaneous intracranial EEG for interictal spike detection and localization. Epilepsy Res 98(2–3):166–173PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Laurent Koessler
    • 1
    • 2
    • 3
  • Thierry Cecchin
    • 1
    • 2
  • Sophie Colnat-Coulbois
    • 4
  • Jean-Pierre Vignal
    • 1
    • 2
    • 3
  • Jacques Jonas
    • 1
    • 2
    • 3
  • Hervé Vespignani
    • 1
    • 2
    • 3
  • Georgia Ramantani
    • 1
    • 2
    • 5
  • Louis Georges Maillard
    • 1
    • 2
    • 3
  1. 1.UMR 7039, CRANCNRS - Université de LorraineVandoeuvre-Lès-NancyFrance
  2. 2.UMR 7039, CRANCNRSVandoeuvre-Lès-NancyFrance
  3. 3.Service de NeurologieCentre Hospitalier Universitaire de NancyNancyFrance
  4. 4.Service de NeurochirurgieCentre Hospitalier Universitaire de NancyNancyFrance
  5. 5.Epilepsy CenterUniversity Hospital FreiburgFreiburgGermany

Personalised recommendations