Artículos de revistas
Pattern Changes Of Eeg Oscillations And Bold Signals Associated With Temporal Lobe Epilepsy As Revealed By A Working Memory Task
Registro en:
Bmc Neuroscience. Biomed Central Ltd., v. 15, n. , p. - , 2014.
14712202
10.1186/1471-2202-15-52
2-s2.0-84899975366
Autor
Ozelo H.F.B.
Alessio A.
Sercheli M.S.
Bilevicius E.
Pedro T.
Pereira F.R.S.
Rondina J.M.
Damasceno B.P.
Cendes F.
Covolan R.J.M.
Institución
Resumen
Background: It is known that the abnormal neural activity in epilepsy may be associated to the reorganization of neural circuits and brain plasticity in various ways. On that basis, we hypothesized that changes in neuronal circuitry due to epilepsy could lead to measurable variations in patterns of both EEG and BOLD signals in patients performing some cognitive task as compared to what would be obtained in normal condition. Thus, the aim of this study was to compare the cerebral areas involved in EEG oscillations versus fMRI signal patterns during a working memory (WM) task in normal controls and patients with refractory mesial temporal lobe epilepsy (MTLE) associated with hippocampal sclerosis (HS). The study included six patients with left MTLE-HS (left-HS group) and seven normal controls (control group) matched to the patients by age and educational level, both groups undergoing a blocked design paradigm based on Sternberg test during separated EEG and fMRI sessions. This test consisted of encoding and maintenance of a variable number of consonant letters on WM. Results: EEG analysis for the encoding period revealed the presence of theta and alpha oscillations in the frontal and parietal areas, respectively. Likewise, fMRI showed the co-occurrence of positive and negative BOLD signals in both brain regions. As for the maintenance period, whereas EEG analysis revealed disappearance of theta oscillation, fMRI showed decrease of positive BOLD in frontal area and increase of negative BOLD in the posterior part of the brain. Conclusions: Generally speaking, these patterns of electrophysiological and hemodynamic signals were observed for both control and left-HS groups. However, the data also revealed remarkable differences between these groups that are consistent with the hypothesis of reorganization of brain circuitry associated with epilepsy. © 2014 Ozelo et al.; licensee BioMed Central Ltd. 15
Gibbs, F.A., Gibbs, E.L., Lennox, W.G., Epilepsy, a paroxysmal cerebral dysrhythmia (1937) Brain, 60, pp. 377-388 Gibbs, F.A., Gibbs, E.L., Lennox, W.G., Electroencephalographic classification of epileptic patients and control subjects (1943) Arch Neurol (Chicago), 50, pp. 111-128 Pfurtscheller, G., Lopes da Silva, F.H., Event-related EEG/MEG synchronization and desynchronization: basic principles (1999) Clin Neurophysiol, 110, pp. 1842-1857. , 10.1016/S1388-2457(99)00141-8, 10576479 Babiloni, C., Pizzella, V., Gratta, C.D., Ferretti, A., Romani, G.L., Fundamentals of electroencefalography, magnetoencefalography, and functional magnetic resonance imaging (2009) Int Rev Neurobiol, 86, pp. 67-80 Smith, S.J.M., EEG in the diagnosis, classification, and management of patients with epilepsy (2005) J Neurol Neurosurg Psychiatry, 76, pp. ii2-ii7. , 1765691, 15961864 Blamire, A., Ogawa, S., Ugurbil, K., Rothman, D., McCarthy, G., Ellermann, J.M., Hyder, F., Shulman, R.G., Dynamic mapping of the human visual cortex by high-speed resonance imaging (1992) Proc Natl Acad Sci U S A, 89, pp. 11060-11073 Hinke, R.M., Hu, X., Stillman, A.E., Kim, S.G., Merkle, K., Salmi, R., Ugurbil, K., Magnetic resonance functional imaging of Broca's area during internal speech (1993) Neuroreport, 4, pp. 675-678. , 10.1097/00001756-199306000-00018, 8347806 Kim, S.G., Ashe, J., Georgopoulos, A.P., Merkle, K., Ellermann, J.M., Menon, R.S., Ogawa, S., Ugurbil, K., Functional imaging of human motor cortex at high magnetic field (1993) J Neurophysiol, 69, pp. 297-302 Kim, S.G., Ashe, J., Hendrich, K., Ellermann, J.M., Merkle, K., Ugurbil, K., Georgopoulos, A.P., Functional magnetic resonance imaging of motor cortex: Hemispheric asymmetry and handedness (1993) Science, 261, pp. 615-617. , 10.1126/science.8342027, 8342027 Kim, S.G., Ugurbil, K., Functional magnetic resonance imaging of the human brain (1997) J Neurosci Methods, 74, pp. 229-243. , 10.1016/S0165-0270(97)02252-8, 9219891 Kim, S.G., Ogawa, S., Insights into new techniques for high resolution functional MRI (2002) Curr Opin Neurobiol, 12, pp. 607-615. , 10.1016/S0959-4388(02)00355-0, 12367643 Logothetis, N.K., Pauls, J., Augath, M., Trinath, T., Oeltermann, A., Neurophysiological investigation of the basis of the fMRI signal (2001) Nature, 412, pp. 150-157. , 10.1038/35084005, 11449264 Hamandi, K., Salek-Haddadi, A., Fish, D.R., Lemieux, L., EEG/functional MR in epilepsy: the Queen Square experience (2004) J Clin Neurophysiol, 21, pp. 241-248. , 10.1097/00004691-200407000-00002, 15509913 Kaufmann, C., Wehrle, R., Wetter, T.C., Holsboer, F., Auer, D.P., Pollmächer, T., Czisch, M., Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study - its limitations and an alternative approach (2006) Brain, 129, pp. 655-667. , 10.1093/brain/awh686, 16339798 Meltzer, J.A., Negishi, M., Mayes, L.C., Constable, R.T., Individual differences in EEG theta and alpha dynamics during working memory correlate with fMRI responses across subjects (2007) Clin Neurophysiol, 118, pp. 2419-2436. , 10.1016/j.clinph.2007.07.023, 2080790, 17900976 Gotman, J., Epileptic networks studied with EEG-fMRI (2008) Epilepsia, 49, pp. 42-51 Scheeringa, R., Petersson, K.M., Oostenveld, R., Norris, D.G., Hagoort, P., Bastiaansen, M.C., Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintenance (2009) Neuroimage, 44, pp. 1224-1238. , 10.1016/j.neuroimage.2008.08.041, 18840533 Laufs, H., A personalized history of EEG-fMRI integration (2012) Neuroimage, 62, pp. 1056-1067. , 10.1016/j.neuroimage.2012.01.039, 22266176 Mandelkow, H., Brandeis, D., Boesiger, P., Good practices in EEG-MRI: the utility of retrospective synchronization and PCA for the removal of MRI gradients artifacts (2010) Neuroimage, 49, pp. 2287-2303. , 10.1016/j.neuroimage.2009.10.050, 19892021 Noth, U., Laufs, H., Stoermer, R., Deichmann, R., Simultaneous electroencephalografy-functional MRI at 3 T: an analysis of safety risks imposed by performing anatomical references scans with the EEG equipment in place (2012) J Magn Reson Imaging, 35, pp. 561-571. , 10.1002/jmri.22843, 22002900 Mullinger, K.J., Castellone, P., Bowtell, R., Best current practice for obtaining high quality EEG data during simultaneous fMRI (2013) J Vis Exp, 76, pp. e50283. , doi:10.3791/50283 Michels, L., Bucher, K., Lüchinger, R., Klaver, P., Martin, E., Jeanmonod, D., Brandeis, D., Simultaneous EEG-fMRI during a working memory task: modulations in low and high frequency bands (2010) PLoS One, 5 (4), pp. e10298. , doi:10.1371/journal.pone.0010298, 10.1371/journal.pone.0010298, 2858659, 20421978 Michels, L., Lüchinger, R., Koenig, T., Martin, E., Brandeis, D., Developmental changes of BOLD signal correlations with global human EEG power and synchronization during working memory (2012) PLoS One, 7 (7), pp. e39447. , doi:10.1371/journal.pone.0039447, 10.1371/journal.pone.0039447, 3391196, 22792176 Cave, C.B., Squire, L.R., Intact verbal and nonverbal short-term memory following damage of the human hippocampus (1992) Hippocampus, 2, pp. 151-163. , 10.1002/hipo.450020207, 1308180 Stretton, J., Thompson, P.J., Frontal lobe function in temporal lobe epilepsy (2012) Epilepsy Res, 98 (1), pp. 1-13. , 10.1016/j.eplepsyres.2011.10.009, 3398387, 22100147 Winston, G.P., Stretton, J., Sidhu, M.K., Symms, M.R., Thompson, P.J., Duncan, J.S., Structural correlates of impaired working memory in hippocampal sclerosis (2013) Epilepsia, 54 (7), pp. 1143-1153. , 10.1111/epi.12193, 3806272, 23614459 Kleen, J.K., Scott, R.C., Holmes, G.L., Roberts, D.W., Rundle, M.M., Testorf, M., Lenck-Santini, P.P., Jobst, B.C., Hippocampal interictal epileptiform activity disrupts cognition in humans (2013) Neurology, 81, pp. 18-24. , 10.1212/WNL.0b013e318297ee50, 23685931 Hermann, B.P., Wyler, A.R., Richey, E.T., Wisconsin card sorting test performance in patients with complex partial seizures of temporal-lobe origin (1988) J Clin Exp Neuropsychol, 10, pp. 467-476. , 10.1080/01688638808408253, 3136190 Corcoran, R., Upton, D., A role for the hippocampus in card sorting? (1993) Cortex, 29, pp. 293-304. , 10.1016/S0010-9452(13)80182-7, 8348826 Stretton, J., Winston, G.P., Sidhu, M., Bonelli, S., Centeno, M., Vollmar, C., Cleary, R.A., Duncan, J.S., Disrupted segregation of working memory in temporal lobe epilepsy (2013) Neuroimage Clin, 2, pp. 273-281. , 3777779, 24179782 Duzel, E., Hufnagel, A., Helmstaedter, C., Elger, C., Verbal working memory components can be selectively influenced by transcranial magnetic stimulation in patients with left temporal lobe epilepsy (1996) Neuropsychologia, 34, pp. 775-783. , 10.1016/0028-3932(95)00160-3, 8817507 Abrahams, S., Morris, R.G., Polkey, C.E., Jarosz, J.M., Cox, T.C., Graves, M., Pickering, A., Hippocampal involvement in spatial and working memory, a structural MRI analysis of patients with unilateral mesial temporal lobe sclerosis (1999) Brain Cogn, 41, pp. 39-65. , 10.1006/brcg.1999.1095, 10536085 Alessio, A., Pereira, F.R.S., Sercheli, M.S., Rondina, J.M., Ozelo, H.B., Bilevicius, E., Pedro, T., Cendes, F., Brain plasticity for verbal and visual memories in patients with mesial temporal lobe epilepsy and hippocampal sclerosis: an fMRI study (2013) Hum Brain Mapp, 34, pp. 186-199. , 10.1002/hbm.21432, 22038783 Bonilha, L., Kobayashi, E., Cendes, F., Li, L.M., Protocol for volumetric segmentation of medial temporal structures using high resolution 3D MRI (2004) Hum Brain Mapp, 22, pp. 145-154. , 10.1002/hbm.20023, 15108302 Sternberg, S., High-speed scanning in human memory (1966) Science, 153, pp. 652-654. , 10.1126/science.153.3736.652, 5939936 Delorme, A., Makeig, S., EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis (2004) J Neurosci Methods, 134, pp. 9-21. , 10.1016/j.jneumeth.2003.10.009, 15102499 Pereira, F.R., Alessio, A., Sercheli, M.S., Pedro, T., Bilevicius, E., Rondina, J.M., Ozelo, H.F., Cendes, F., Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI (2010) BMC Neurosci, 11, p. 66. , 10.1186/1471-2202-11-66, 2890013, 20525202 Boynton, G.M., Engel, S.A., Glover, G.H., Heeger, D.J., Linear systems analysis of functional magnetic resonance imaging in human V1 (1996) J Neurosci Offic J Soc Neurosci, 16, pp. 4207-4221 Rajapakse, J.C., Kruggel, F., Maisog, J.M., von Cramon, D.Y., Modeling hemodynamic response for analysis of functional MRI time-series (1998) Hum Brain Mapp, 6, pp. 283-300. , 10.1002/(SICI)1097-0193(1998)6:4<283::AID-HBM7>3.0.CO;2-#, 9704266 Press, W.H., Teukolski, S.A., Vetterling, W.T., Flannery, B.P., (1994) Numerical recipes in C: the art of scientific computing, , Engand: Cambridge Univeristy Press Lieberman, M.D., Cunningham, W.A., Type I and Type II error concerns in fMRI research: re-balancing the scale (2009) Soc Cogn Affect Neurosci, 4, pp. 423-428. , 10.1093/scan/nsp052, 2799956, 20035017 Koessler, L., Maillard, L., Benhadid, A., Vignal, J.P., Felblinger, J., Vespignani, H., Braun, M., Autometed cortical projection of EEG sensors: Anatomical correlation via the international 10-20 system (2009) Neuroimage, 46, pp. 64-72. , 10.1016/j.neuroimage.2009.02.006, 19233295 Tudesco, I.S.S., Vaz, L.J., Mantoan, M.A.S., Beizunces, E., Noffs, M.H., Caboclo, L.O.S.F., Yacubian, E.M.T., Bueno, O.F.A., Assessment of working memory in patients with mesial temporal lobe epilepsy associated with unilateral hippocampal sclerosis (2010) Epilepsy Behav, 18, pp. 223-228. , 10.1016/j.yebeh.2010.04.021, 20547107 Gevins, A., Smith, M.E., McEvoy, L., Yu, D., High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice (1997) Cereb Cortex, 7, pp. 374-385. , 10.1093/cercor/7.4.374, 9177767 Onton, J., Delorme, A., Makeig, S., Frontal midline EEG dynamics during working memory (2005) Neuroimage, 27, pp. 341-356. , 10.1016/j.neuroimage.2005.04.014, 15927487 Hsieh, L.T., Ranganath, C., Frontal midline theta oscillations during working memory maintenance and episodic encoding and retrieval (2013) Neuroimage, , in press Ishihara, T., Yoshi, N., Multivariate analytic study of EEG and mental activity in juvenile delinquents (1972) Electroencephalogr Clin Neurophysiol, 33, pp. 71-80. , 10.1016/0013-4694(72)90026-0, 4113276 Roberts, B.M., Hsieh, L.T., Ranganath, C., Oscillatory activity during maintenance of spatial and temporal information in working memory (2013) Neuropsychologia, 51, pp. 349-357. , 10.1016/j.neuropsychologia.2012.10.009, 3546228, 23084981 Harmony, T., Fernández, T., Gersenowies, J., Galán, L., Fernández-Bouzas, A., Aubert, E., Díaz-Comas, L., Specific EEG frequencies signal general common cognitive processes as well as specific task processes in man (2004) Int J Psychophysiol, 53, pp. 207-216. , 10.1016/j.ijpsycho.2004.04.006, 15246674 Harmony, T., The functional significance of delta oscillations in cognitive processing (2013) Front Integr Neurosci, 7, p. 83. , eCollection 2013, 3851789, 24367301 Freunberger, R., Werkle-Bergner, M., Griesmayr, B., Lindenberger, U., Klimesch, W., Brain oscillatory correlates of working memory constraints (2011) Brain Res, 1375, pp. 93-102 Roux, F., Uhlhaas, P.J., Working memory and neural oscillations: alpha-gamma versus theta-gamma codes for distinct WM information? (2014) Trends Cogn Sci, 18 (1), pp. 16-25. , doi:10.1016/j.tics.2013.10.010, 10.1016/j.tics.2013.10.010, 24268290 Fox, M.D., Snyder, A.Z., Vincent, J.L., Corbetta, M., Van Essen, D.C., Raichle, M.E., The human brain is intrinsically organized into dynamic, anticorrelated functional networks (2005) Proc Natl Acad Sci U S A, 102, pp. 9673-9678. , 10.1073/pnas.0504136102, 1157105, 15976020 Fransson, P., Spontaneous low-frequency BOLD signal fluctuations: An fMRI investigation of the resting-state default mode of brain function hypothesis (2005) Hum Brain Mapp, 26, pp. 15-29. , 10.1002/hbm.20113, 15852468 Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L., A default mode of brain function (2001) Proc Natl Acad Sci U S A, 98, pp. 676-682. , 10.1073/pnas.98.2.676, 14647, 11209064 Kopell, N., Whittington, M.A., Kramer, M.A., Neuronal assembly dynamics in the beta1 frequency range permits short-term memory (2011) Proc Natl Acad Sci U S A, 9, pp. 3779-3784 Powell, H.W., Richardson, M.P., Symms, M.R., Boulby, P.A., Thompson, P.J., Duncan, J.S., Koepp, M.J., Reorganization of verbal and nonverbal memory in temporal lobe epilepsy due to unilateral hippocampal sclerosis (2007) Epilepsia, 48, pp. 1512-1525. , 10.1111/j.1528-1167.2007.01053.x, 2913101, 17430404 Guedj, E., Bettus, G., Barbeau, E.J., Liegeois-Chauvel, C., Confort-Gouny, S., Bartolomei, F., Chauvel, P., Guye, M., Hyperactivation of parahippocampal region and fusiform gyrus associated with successful encoding in medial temporal lobe epilepsy (2011) Epilepsia, 52, pp. 1100-1109. , 10.1111/j.1528-1167.2011.03052.x, 21480879 Bonilha, L., Nesland, T., Martz, G.U., Joseph, J.E., Spampinato, M.V., Edwards, J.C., Tabesh, A., Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures (2012) J Neurol Neurosurg Psychiatry, 83, pp. 903-909. , 10.1136/jnnp-2012-302476, 3415309, 22764263 Campo, P., Garrido, M.I., Moran, R.J., García-Morales, I., Poch, C., Toledano, R., Gil-Nagel, A., Friston, K.J., Network reconfiguration and working memory impairment in mesial temporal lobe epilepsy (2013) Neuroimage, 72, pp. 48-54. , 3610031, 23370058 Detre, J.A., Maccotta, L., King, D., Alsop, D.C., Glosser, G., D'Esposito, M., Zarahn, E., French, J.A., Functional MRI lateralization of memory in temporal lobe epilepsy (1998) Neurology, 50, pp. 926-932. , 10.1212/WNL.50.4.926, 9566374 Szaflarski, J.P., Holland, S.K., Schmithorst, V.J., Dunn, R.S., Privitera, M.D., High-resolution functional MRI at 3 T in health and epilepsy subjects: Hippocampal activation with picture encoding task (2004) Epilepsy Behav, 5, pp. 244-252. , 10.1016/j.yebeh.2004.01.002, 15123027 Stretton, J., Winston, G., Sidhu, M., Centeno, M., Vollmar, C., Bonelli, S., Symms, M., Thompson, P.J., Neural correlates of working memory in Temporal Lobe Epilepsy - an fMRI study (2012) Neuroimage, 60, pp. 1696-1703. , 10.1016/j.neuroimage.2012.01.126, 3677092, 22330313