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.
Similar content being viewed by others
References
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.
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.
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.
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.
Brigo, F., Rossini, F., Stefani, A., Nardone, R., Tezzon, F., Fiaschi, A., et al. (2013). Fixation-off sensitivity. Clinical Neurophysiology, 124(2), 221–227.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Laufs, H. (2008). Endogenous brain oscillations and related networks detected by surface EEG-combined fMRI. Human Brain Mapping, 29(7), 762–769.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Patel, J. K., & Read, C. B. (1996). Handbook of the normal distribution. New York: Marcel Dekker.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Acknowledgments
The authors would like to thank Ricardo Bruña and Elena Molina for productive discussions on the applied analysis in this work. Fudnación CIEN-Fundacion Reina Sofia, Centro de Investigación en red Ciber-BBN, projects MADR.IB S-SAL-312-2006 by Comunidad de Madrid and TEC2009-14587-C03-02 by Spanish Government, Consejo Social of Universidad Politecnica de Madrid and fellowship RR02/2009 (UPM) have provided funds towards this project.
Disclosures
Ana Beatriz Solana Sánchez declares that she is employee of General Electric Global Research Center. However, this research work was carried out while doing her PhD in the Center for Biomedical Technology in Madrid under public funding sources detailed in the acknowledgements.
Kenia Martínez, Juan Antonio Hernández-Tamames, Victoria San Antonio-Arce, Rafael Toledano, Irene García-Morales, Juan Alvárez-Linera, Antonio Gil-Nágel and Francisco del Pozo declare that they have no conflict of interest.
All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 694 kb)
Rights and permissions
About this article
Cite this article
Solana, A.B., Martínez, K., Hernández-Tamames, J.A. et al. Altered brain rhythms and functional network disruptions involved in patients with generalized fixation-off epilepsy. Brain Imaging and Behavior 10, 373–386 (2016). https://doi.org/10.1007/s11682-015-9404-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11682-015-9404-6