Brain Imaging and Behavior

, Volume 10, Issue 2, pp 373–386 | Cite as

Altered brain rhythms and functional network disruptions involved in patients with generalized fixation-off epilepsy

  • Ana Beatriz Solana
  • Kenia Martínez
  • Juan Antonio Hernández-Tamames
  • Victoria San Antonio-Arce
  • Rafael Toledano
  • Irene García-Morales
  • Juan Alvárez-Linera
  • Antonio Gil-Nágel
  • Francisco del Pozo
Original Research

Abstract

Generalized Fixation-off Sensitivity (CGE-FoS) patients present abnormal EEG patterns when losing fixation. In the present work, we studied two CGE-FoS epileptic patients with simultaneous EEG-fMRI. We aim to identify brain areas that are specifically related to the pathology by identifying the brain networks that are related to the EEG brain altered rhythms. Three main analyses were performed: EEG standalone, where the voltage fluctuations in delta, alpha, and beta EEG bands were obtained; fMRI standalone, where resting-state fMRI ICA analyses for opened and closed eyes conditions were computed per subject; and, EEG-informed fMRI, where EEG delta, alpha and beta oscillations were used to analyze fMRI. Patient 1 showed EEG abnormalities for lower beta band EEG brain rhythm. Fluctuations of this rhythm were correlated with a brain network mainly composed by temporo-frontal areas only found in the closed eyes condition. Patient 2 presented alterations in all the EEG brain rhythms (delta, alpha, beta) under study when closing eyes. Several biologically relevant brain networks highly correlated (r > 0.7) to each other in the closed eyes condition were found. EEG-informed fMRI results in patient 2 showed hypersynchronized patterns in the fMRI correlation spatial maps. The obtained findings allow a differential diagnosis for each patient and different profiles with respect to healthy volunteers. The results suggest a different disruption in the functional brain networks of these patients that depends on their altered brain rhythms. This knowledge could be used to treat these patients by novel brain stimulation approaches targeting specific altered brain networks in each patient.

Keywords

Fixation-off Simultaneous EEG-fMRI Resting-state networks EEG-informed fMRI ICA 

Supplementary material

11682_2015_9404_MOESM1_ESM.docx (694 kb)
ESM 1(DOCX 694 kb)

References

  1. Allen, P. J., Josephs, O., & Turner, R. (2000). A method for removing imaging artifact from continuous EEG recorded during functional MRI. NeuroImage, 12(2), 230–239.CrossRefPubMedGoogle Scholar
  2. Beckmann, C. F., DeLuca, M., Devlin, J. T., & Smith, S. M. (2005). Investigations into resting-state connectivity using independent component analysis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 360(1457), 1001–1013.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beckmann, C. F., & Smith, S. M. (2004). Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Transactions on Medical Imaging, 23(2), 137–152.CrossRefPubMedGoogle Scholar
  4. Bittar, R. G., Andermann, F., Olivier, A., Dubeau, F., Dumoulin, S. O., Pike, G. B., & Reutens, D. C. (1999). Interictal spikes increase cerebral glucose metabolism and blood flow: a PET study. Epilepsia, 40(2), 170–178.CrossRefPubMedGoogle Scholar
  5. Brigo, F., Rossini, F., Stefani, A., Nardone, R., Tezzon, F., Fiaschi, A., et al. (2013). Fixation-off sensitivity. Clinical Neurophysiology, 124(2), 221–227.CrossRefPubMedGoogle Scholar
  6. Chaudhary, U. J., Duncan, J. S., & Lemieux, L. (2013). Mapping hemodynamic correlates of seizures using fMRI: a review. Human Brain Mapping, 34(2), 447–466.CrossRefPubMedGoogle Scholar
  7. Damoiseaux, J. S., Rombouts, S. A., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., & Beckmann, C. F. (2006). Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences of the United States of America, 103(37), 13848–13853.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Di Bonaventura, C., Vaudano, A. E., Carni, M., Pantano, P., Nucciarelli, V., Garreffa, G., et al. (2005). Long-term reproducibility of fMRI activation in epilepsy patients with fixation off sensitivity. Epilepsia, 46(7), 1149–1151.CrossRefPubMedGoogle Scholar
  9. Feige, B., Scheffler, K., Esposito, F., Di Salle, F., Hennig, J., & Seifritz, E. (2005). Cortical and subcortical correlates of electroencephalographic alpha rhythm modulation. Journal of Neurophysiology, 93(5), 2864–2872.CrossRefPubMedGoogle Scholar
  10. Formaggio, E., Storti, S. F., Boscolo Galazzo, I., Bongiovanni, L. G., Cerini, R., Fiaschi, A., & Manganotti, P. (2013). Reproducibility of EEG-fMRI results in a patient with fixation-off sensitivity. Clin EEG Neurosci.Google Scholar
  11. Goldman, R. I., Stern, J. M., Engel, J., Jr., & Cohen, M. S. (2002). Simultaneous EEG and fMRI of the alpha rhythm. Neuroreport, 13(18), 2487–2492.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Iannetti, G. D., Di Bonaventura, C., Pantano, P., Giallonardo, A. T., Romanelli, P. L., Bozzao, L., et al. (2002). fMRI/EEG in paroxysmal activity elicited by elimination of central vision and fixation. Neurology, 58(6), 976–979.CrossRefPubMedGoogle Scholar
  13. Jann, K., Dierks, T., Boesch, C., Kottlow, M., Strik, W., & Koenig, T. (2009). BOLD correlates of EEG alpha phase-locking and the fMRI default mode network. NeuroImage, 45(3), 903–916.CrossRefPubMedGoogle Scholar
  14. Kelly, R. E., Jr., Alexopoulos, G. S., Wang, Z., Gunning, F. M., Murphy, C. F., Morimoto, S. S., et al. (2010). Visual inspection of independent components: defining a procedure for artifact removal from fMRI data. Journal of Neuroscience Methods, 189(2), 233–245.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Klimesch, W. (1999). EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Research. Brain Research Reviews, 29(2–3), 169–195.CrossRefPubMedGoogle Scholar
  16. Koutroumanidis, M., Tsatsou, K., Sanders, S., Michael, M., Tan, S. V., Agathonikou, A., & Panayiotopoulos, C. P. (2009). Fixation-off sensitivity in epilepsies other than the idiopathic epilepsies of childhood with occipital paroxysms: a 12-year clinical-video EEG study. Epileptic Disorders, 11(1), 20–36.PubMedGoogle Scholar
  17. Krakow, K., Baxendale, S. A., Maguire, E. A., Krishnamoorthy, E. S., Lemieux, L., Scott, C. A., & Smith, S. J. (2000). Fixation-off sensitivity as a model of continuous epileptiform discharges: electroencephalographic, neuropsychological and functional MRI findings. Epilepsy Research, 42(1), 1–6.CrossRefPubMedGoogle Scholar
  18. Laufs, H. (2008). Endogenous brain oscillations and related networks detected by surface EEG-combined fMRI. Human Brain Mapping, 29(7), 762–769.CrossRefPubMedGoogle Scholar
  19. Laufs, H., Daunizeau, J., Carmichael, D. W., & Kleinschmidt, A. (2008). Recent advances in recording electrophysiological data simultaneously with magnetic resonance imaging. NeuroImage, 40(2), 515–528.CrossRefPubMedGoogle Scholar
  20. Laufs, H., Kleinschmidt, A., Beyerle, A., Eger, E., Salek-Haddadi, A., Preibisch, C., & Krakow, K. (2003). EEG-correlated fMRI of human alpha activity. NeuroImage, 19(4), 1463–1476.CrossRefPubMedGoogle Scholar
  21. Mandelkow, H., Halder, P., Boesiger, P., & Brandeis, D. (2006). Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth. NeuroImage, 32(3), 1120–1126.CrossRefPubMedGoogle Scholar
  22. Mantini, D., Perrucci, M. G., Del Gratta, C., Romani, G. L., & Corbetta, M. (2007). Electrophysiological signatures of resting state networks in the human brain. Proceedings of the National Academy of Sciences of the United States of America, 104(32), 13170–13175.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Martinez, K., Solana, A. B., Burgaleta, M., Hernandez-Tamames, J. A., Alvarez-Linera, J., Roman, F. J., et al. (2013). Changes in resting-state functionally connected parietofrontal networks after videogame practice. Human Brain Mapping, 34(12), 3143–3157.CrossRefPubMedGoogle Scholar
  24. Mecarelli, O., Gregori, B., Gilio, F., Conte, A., Frasca, V., Accornero, N., & Inghilleri, M. (2006). Effects of repetitive transcranial magnetic stimulation in a patient with fixation-off sensitivity. Experimental Brain Research, 173(1), 180–184.CrossRefPubMedGoogle Scholar
  25. Michels, L., Bucher, K., Luchinger, R., Klaver, P., Martin, E., Jeanmonod, D., & Brandeis, D. (2010). Simultaneous EEG-fMRI during a working memory task: modulations in low and high frequency bands. PLoS One, 5(4), e10298.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Parra, J., Meeren, H. K., Kalitzin, S., Suffczynski, P., de Munck, J. C., Harding, G. F., et al. (2000a). Magnetic source imaging in fixation-off sensitivity: relationship with alpha rhythm. Journal of Clinical Neurophysiology, 17(2), 212–223.CrossRefPubMedGoogle Scholar
  27. Parra, J., Meeren, H. K., Kalitzin, S., Suffczynski, P., de Munck, J. C., Harding, G. F., et al. (2000b). Magnetic source imaging in fixation-off sensitivity: relationship with alpha rhythm. Journal of Clinical Neurophysiology, 17(2), 212–223.CrossRefPubMedGoogle Scholar
  28. Patel, J. K., & Read, C. B. (1996). Handbook of the normal distribution. New York: Marcel Dekker.Google Scholar
  29. Patriat, R., Molloy, E. K., Meier, T. B., Kirk, G. R., Nair, V. A., Meyerand, M. E., et al. (2013). The effect of resting condition on resting-state fMRI reliability and consistency: a comparison between resting with eyes open, closed, and fixated. NeuroImage, 78, 463–473.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Peca, S., Carni, M., Di Bonaventura, C., Aprile, T., Hagberg, G. E., Giallonardo, A. T., et al. (2010). Metabolic correlatives of brain activity in a FOS epilepsy patient. NMR in Biomedicine, 23(2), 170–178.PubMedGoogle Scholar
  31. Smith, S. M., Fox, P. T., Miller, K. L., Glahn, D. C., Fox, P. M., Mackay, C. E., et al. (2009). Correspondence of the brain’s functional architecture during activation and rest. Proceedings of the National Academy of Sciences of the United States of America, 106(31), 13040–13045.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Solana, A. B., Hernandez-Tamames, J. A., Manzanedo, E., Garcia-Alvarez, R., Zelaya, F. O., & Del Pozo, F. (2014). Gradient induced artifacts in simultaneous EEG-fMRI: Effect of synchronization on spiral and EPI k-space trajectories. Magn Reson Imaging.Google Scholar
  33. Srivastava, G., Crottaz-Herbette, S., Lau, K. M., Glover, G. H., & Menon, V. (2005). ICA-based procedures for removing ballistocardiogram artifacts from EEG data acquired in the MRI scanner. NeuroImage, 24(1), 50–60.CrossRefPubMedGoogle Scholar
  34. Strigaro, G., Prandi, P., Varrasi, C., Monaco, F., & Cantello, R. (2011). Cortical excitability changes associated with fixation-off sensitivity: a case report. Epilepsia, 52(8), e89–92.CrossRefPubMedGoogle Scholar
  35. Wu, L., Eichele, T., & Calhoun, V. D. (2010). Reactivity of hemodynamic responses and functional connectivity to different states of alpha synchrony: a concurrent EEG-fMRI study. NeuroImage, 52(4), 1252–1260.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Yuan, H., Zotev, V., Phillips, R., Drevets, W. C., & Bodurka, J. (2012). Spatiotemporal dynamics of the brain at rest–exploring EEG microstates as electrophysiological signatures of BOLD resting state networks. NeuroImage, 60(4), 2062–2072.CrossRefPubMedGoogle Scholar
  37. Zuo, X. N., Kelly, C., Adelstein, J. S., Klein, D. F., Castellanos, F. X., & Milham, M. P. (2010). Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. NeuroImage, 49(3), 2163–2177.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Ana Beatriz Solana
    • 1
    • 7
  • Kenia Martínez
    • 2
  • Juan Antonio Hernández-Tamames
    • 3
  • Victoria San Antonio-Arce
    • 4
  • Rafael Toledano
    • 5
  • Irene García-Morales
    • 5
  • Juan Alvárez-Linera
    • 6
  • Antonio Gil-Nágel
    • 5
  • Francisco del Pozo
    • 1
  1. 1.Department of Neuroimaging, Center for Biomedical TechnologyUniversidad Politécnica de MadridPozuelo de AlarcónSpain
  2. 2.Research Unit, Instituto de Investigación Sanitaria del Hospital Gregorio Marañón (IISGM)MadridSpain
  3. 3.Department of Electronical TechnologyUniversidad Rey Juan CarlosMóstolesSpain
  4. 4.Epilepsy CenterUniversity Hospital FreiburgFreiburgGermany
  5. 5.Department of NeurologyHospital Ruber InternacionalMadridSpain
  6. 6.Department of NeuroradiologyHospital Ruber InternacionalMadridSpain
  7. 7.GE Global ResearchGarching bei MunichGermany

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