Skip to main content
Top
Published in: Brain Topography 6/2015

01-11-2015 | Original Paper

Quantification of Interictal Neuromagnetic Activity in Absence Epilepsy with Accumulated Source Imaging

Authors: Jing Xiang, Jeffrey R. Tenney, Abraham M. Korman, Kimberly Leiken, Douglas F. Rose, Elana Harris, Weihong Yuan, Paul S. Horn, Katherine Holland, David W. Loring, Tracy A. Glauser

Published in: Brain Topography | Issue 6/2015

Login to get access

Abstract

Aberrant brain activity in childhood absence epilepsy (CAE) during seizures has been well recognized as synchronous 3 Hz spike-and-wave discharges on electroencephalography. However, brain activity from low- to very high-frequency ranges in subjects with CAE between seizures (interictal) has rarely been studied. Using a high-sampling rate magnetoencephalography (MEG) system, we studied ten subjects with clinically diagnosed but untreated CAE in comparison with age- and gender-matched controls. MEG data were recorded from all subjects during the resting state. MEG sources were assessed with accumulated source imaging, a new method optimized for localizing and quantifying spontaneous brain activity. MEG data were analyzed in nine frequency bands: delta (1–4 Hz), theta (4–8 Hz), alpha (8–12 Hz), beta (12–30 Hz), low-gamma (30–55 Hz), high-gamma (65–90 Hz), ripple (90–200 Hz), high-frequency oscillation (HFO, 200–1,000 Hz), and very high-frequency oscillation (VHFO, 1,000–2,000 Hz). MEG source imaging revealed that subjects with CAE had higher odds of interictal brain activity in 200–1,000 and 1,000–2,000 Hz in the parieto-occipito-temporal junction and the medial frontal cortices as compared with controls. The strength of the interictal brain activity in these regions was significantly elevated in the frequency bands of 90–200, 200–1,000 and 1,000–2,000 Hz for subjects with CAE as compared with controls. The results indicate that CAE has significantly aberrant brain activity between seizures that can be noninvasively detected. The measurements of high-frequency neuromagnetic oscillations may open a new window for investigating the cerebral mechanisms of interictal abnormalities in CAE.
Literature
go back to reference Amor F, Baillet S, Navarro V, Adam C, Martinerie J, Quyen Mle V (2009) Cortical local and long-range synchronization interplay in human absence seizure initiation. Neuroimage 45(3):950–962CrossRefPubMed Amor F, Baillet S, Navarro V, Adam C, Martinerie J, Quyen Mle V (2009) Cortical local and long-range synchronization interplay in human absence seizure initiation. Neuroimage 45(3):950–962CrossRefPubMed
go back to reference Bai X, Guo J, Killory B, Vestal M, Berman R, Negishi M, Danielson N, Novotny EJ, Constable RT, Blumenfeld H (2011) Resting functional connectivity between the hemispheres in childhood absence epilepsy. Neurology 76(23):1960–1967PubMedCentralCrossRefPubMed Bai X, Guo J, Killory B, Vestal M, Berman R, Negishi M, Danielson N, Novotny EJ, Constable RT, Blumenfeld H (2011) Resting functional connectivity between the hemispheres in childhood absence epilepsy. Neurology 76(23):1960–1967PubMedCentralCrossRefPubMed
go back to reference Bragin A, Wilson CL, Almajano J, Mody I, Engel J Jr (2004) High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia 45(9):1017–1023CrossRefPubMed Bragin A, Wilson CL, Almajano J, Mody I, Engel J Jr (2004) High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia 45(9):1017–1023CrossRefPubMed
go back to reference Brookes MJ, Stevenson CM, Barnes GR, Hillebrand A, Simpson MI, Francis ST, Morris PG (2007) Beamformer reconstruction of correlated sources using a modified source model. Neuroimage 34(4):1454–1465CrossRefPubMed Brookes MJ, Stevenson CM, Barnes GR, Hillebrand A, Simpson MI, Francis ST, Morris PG (2007) Beamformer reconstruction of correlated sources using a modified source model. Neuroimage 34(4):1454–1465CrossRefPubMed
go back to reference Caraballo RH, Darra F, Fontana E, Garcia R, Monese E, Dalla Bernardina B (2011) Absence seizures in the first 3 years of life: an electroclinical study of 46 cases. Epilepsia 52(2):393–400PubMed Caraballo RH, Darra F, Fontana E, Garcia R, Monese E, Dalla Bernardina B (2011) Absence seizures in the first 3 years of life: an electroclinical study of 46 cases. Epilepsia 52(2):393–400PubMed
go back to reference Ebersole JS, Ebersole SM (2010) Combining MEG and EEG source modeling in epilepsy evaluations. J Clin Neurophysiol 27(6):360–371CrossRefPubMed Ebersole JS, Ebersole SM (2010) Combining MEG and EEG source modeling in epilepsy evaluations. J Clin Neurophysiol 27(6):360–371CrossRefPubMed
go back to reference Engel J Jr, Bragin A, Staba R, Mody I (2009) High-frequency oscillations: what is normal and what is not? Epilepsia 50(4):598–604CrossRefPubMed Engel J Jr, Bragin A, Staba R, Mody I (2009) High-frequency oscillations: what is normal and what is not? Epilepsia 50(4):598–604CrossRefPubMed
go back to reference Epilepsy CoCaTotILA (1989) Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League against Epilepsy. Epilepsia 30(4):389–399CrossRef Epilepsy CoCaTotILA (1989) Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League against Epilepsy. Epilepsia 30(4):389–399CrossRef
go back to reference Fischer MJ, Rampp S, Scheler G, Stefan H (2008) A systematic review on MEG and its use in the presurgical evaluation of localization-related epilepsy. Epilepsy Res 82(2–3):238–239 author reply 240–231CrossRefPubMed Fischer MJ, Rampp S, Scheler G, Stefan H (2008) A systematic review on MEG and its use in the presurgical evaluation of localization-related epilepsy. Epilepsy Res 82(2–3):238–239 author reply 240–231CrossRefPubMed
go back to reference Glauser TA, Cnaan A, Shinnar S, Hirtz DG, Dlugos D, Masur D, Clark PO, Capparelli EV, Adamson PC, Childhood Absence Epilepsy Study G (2010) Ethosuximide, valproic acid, and lamotrigine in childhood absence epilepsy. N Engl J Med 362(9):790–799CrossRef Glauser TA, Cnaan A, Shinnar S, Hirtz DG, Dlugos D, Masur D, Clark PO, Capparelli EV, Adamson PC, Childhood Absence Epilepsy Study G (2010) Ethosuximide, valproic acid, and lamotrigine in childhood absence epilepsy. N Engl J Med 362(9):790–799CrossRef
go back to reference Haegelen C, Perucca P, Chatillon CE, Andrade-Valenca L, Zelmann R, Jacobs J, Collins DL, Dubeau F, Olivier A, Gotman J (2013) High-frequency oscillations, extent of surgical resection, and surgical outcome in drug-resistant focal epilepsy. Epilepsia 54(5):848–857PubMedCentralCrossRefPubMed Haegelen C, Perucca P, Chatillon CE, Andrade-Valenca L, Zelmann R, Jacobs J, Collins DL, Dubeau F, Olivier A, Gotman J (2013) High-frequency oscillations, extent of surgical resection, and surgical outcome in drug-resistant focal epilepsy. Epilepsia 54(5):848–857PubMedCentralCrossRefPubMed
go back to reference Huang MX, Theilmann RJ, Robb A, Angeles A, Nichols S, Drake A, D’Andrea J, Levy M, Holland M, Song T, Ge S, Hwang E, Yoo K, Cui L, Baker DG, Trauner D, Coimbra R, Lee RR (2009) Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients. J Neurotrauma 26(8):1213–1226CrossRefPubMed Huang MX, Theilmann RJ, Robb A, Angeles A, Nichols S, Drake A, D’Andrea J, Levy M, Holland M, Song T, Ge S, Hwang E, Yoo K, Cui L, Baker DG, Trauner D, Coimbra R, Lee RR (2009) Integrated imaging approach with MEG and DTI to detect mild traumatic brain injury in military and civilian patients. J Neurotrauma 26(8):1213–1226CrossRefPubMed
go back to reference Hughes SW, Lorincz ML, Parri HR, Crunelli V (2011) Infraslow (<0.1 Hz) oscillations in thalamic relay nuclei basic mechanisms and significance to health and disease states. Prog Brain Res 193:145–162PubMedCentralCrossRefPubMed Hughes SW, Lorincz ML, Parri HR, Crunelli V (2011) Infraslow (<0.1 Hz) oscillations in thalamic relay nuclei basic mechanisms and significance to health and disease states. Prog Brain Res 193:145–162PubMedCentralCrossRefPubMed
go back to reference Jacobs J, Staba R, Asano E, Otsubo H, Wu JY, Zijlmans M, Mohamed I, Kahane P, Dubeau F, Navarro V, Gotman J (2012) High-frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol 98(3):302–315PubMedCentralCrossRefPubMed Jacobs J, Staba R, Asano E, Otsubo H, Wu JY, Zijlmans M, Mohamed I, Kahane P, Dubeau F, Navarro V, Gotman J (2012) High-frequency oscillations (HFOs) in clinical epilepsy. Prog Neurobiol 98(3):302–315PubMedCentralCrossRefPubMed
go back to reference Kerber K, Dumpelmann M, Schelter B, LeVan P, Korinthenberg R, Schulze-Bonhage A, Jacobs J (2014) Differentiation of specific ripple patterns helps to identify epileptogenic areas for surgical procedures. Clin Neurophysiol 125(7):1339–45 Kerber K, Dumpelmann M, Schelter B, LeVan P, Korinthenberg R, Schulze-Bonhage A, Jacobs J (2014) Differentiation of specific ripple patterns helps to identify epileptogenic areas for surgical procedures. Clin Neurophysiol 125(7):1339–45
go back to reference Killory BD, Bai X, Negishi M, Vega C, Spann MN, Vestal M, Guo J, Berman R, Danielson N, Trejo J, Shisler D, Novotny EJ Jr, Constable RT, Blumenfeld H (2011) Impaired attention and network connectivity in childhood absence epilepsy. Neuroimage 56(4):2209–2217PubMedCentralCrossRefPubMed Killory BD, Bai X, Negishi M, Vega C, Spann MN, Vestal M, Guo J, Berman R, Danielson N, Trejo J, Shisler D, Novotny EJ Jr, Constable RT, Blumenfeld H (2011) Impaired attention and network connectivity in childhood absence epilepsy. Neuroimage 56(4):2209–2217PubMedCentralCrossRefPubMed
go back to reference Lopes da Silva FH, Blanes W, Kalitzin SN, Parra J, Suffczynski P, Velis DN (2003) Dynamical diseases of brain systems: different routes to epileptic seizures. IEEE Trans Bio-Med Eng 50(5):540–548CrossRef Lopes da Silva FH, Blanes W, Kalitzin SN, Parra J, Suffczynski P, Velis DN (2003) Dynamical diseases of brain systems: different routes to epileptic seizures. IEEE Trans Bio-Med Eng 50(5):540–548CrossRef
go back to reference Mariani E, Rossi LN, Vajani S (2011) Interictal paroxysmal EEG abnormalities in childhood absence epilepsy. Seizure 20(4):299–304CrossRefPubMed Mariani E, Rossi LN, Vajani S (2011) Interictal paroxysmal EEG abnormalities in childhood absence epilepsy. Seizure 20(4):299–304CrossRefPubMed
go back to reference Menendez de la Prida L, Trevelyan AJ (2011) Cellular mechanisms of high frequency oscillations in epilepsy: on the diverse sources of pathological activities. Epilepsy Res 97(3):308–317CrossRefPubMed Menendez de la Prida L, Trevelyan AJ (2011) Cellular mechanisms of high frequency oscillations in epilepsy: on the diverse sources of pathological activities. Epilepsy Res 97(3):308–317CrossRefPubMed
go back to reference Miao A, Xiang J, Tang L, Ge H, Liu H, Wu T, Chen Q, Hu Z, Lu X, Wang X (2014) Using ictal high-frequency oscillations (80–500 Hz) to localize seizure onset zones in childhood absence epilepsy: a MEG study. Neurosci Lett 566:21–26CrossRefPubMed Miao A, Xiang J, Tang L, Ge H, Liu H, Wu T, Chen Q, Hu Z, Lu X, Wang X (2014) Using ictal high-frequency oscillations (80–500 Hz) to localize seizure onset zones in childhood absence epilepsy: a MEG study. Neurosci Lett 566:21–26CrossRefPubMed
go back to reference Moeller F, LeVan P, Muhle H, Stephani U, Dubeau F, Siniatchkin M, Gotman J (2010) Absence seizures: individual patterns revealed by EEG-fMRI. Epilepsia 51(10):2000–2010PubMedCentralCrossRefPubMed Moeller F, LeVan P, Muhle H, Stephani U, Dubeau F, Siniatchkin M, Gotman J (2010) Absence seizures: individual patterns revealed by EEG-fMRI. Epilepsia 51(10):2000–2010PubMedCentralCrossRefPubMed
go back to reference Mullen SA, Suls A, De Jonghe P, Berkovic SF, Scheffer IE (2010) Absence epilepsies with widely variable onset are a key feature of familial GLUT1 deficiency. Neurology 75(5):432–440CrossRefPubMed Mullen SA, Suls A, De Jonghe P, Berkovic SF, Scheffer IE (2010) Absence epilepsies with widely variable onset are a key feature of familial GLUT1 deficiency. Neurology 75(5):432–440CrossRefPubMed
go back to reference Ogura K, Maegaki Y, Koeda T (2005) EEG evaluation of fixation-off sensitivity in eyelid myoclonia with absences. Pediatr Neurol 33(2):142–145CrossRefPubMed Ogura K, Maegaki Y, Koeda T (2005) EEG evaluation of fixation-off sensitivity in eyelid myoclonia with absences. Pediatr Neurol 33(2):142–145CrossRefPubMed
go back to reference Ponten SC, Douw L, Bartolomei F, Reijneveld JC, Stam CJ (2009) Indications for network regularization during absence seizures: weighted and unweighted graph theoretical analyses. Exp Neurol 217(1):197–204CrossRefPubMed Ponten SC, Douw L, Bartolomei F, Reijneveld JC, Stam CJ (2009) Indications for network regularization during absence seizures: weighted and unweighted graph theoretical analyses. Exp Neurol 217(1):197–204CrossRefPubMed
go back to reference Rampp S, Stefan H (2007) Magnetoencephalography in presurgical epilepsy diagnosis. Expert Rev Med Devices 4(3):335–347CrossRefPubMed Rampp S, Stefan H (2007) Magnetoencephalography in presurgical epilepsy diagnosis. Expert Rev Med Devices 4(3):335–347CrossRefPubMed
go back to reference Richardson MP (2011) New observations may inform seizure models: very fast and very slow oscillations. Prog Biophys Mol Biol 105(1–2):5–13CrossRefPubMed Richardson MP (2011) New observations may inform seizure models: very fast and very slow oscillations. Prog Biophys Mol Biol 105(1–2):5–13CrossRefPubMed
go back to reference Sheth RD, Abram HS (2010) Absence epilepsy with focal clinical and electrographic seizures. Semin Pediatr Neurol 17(1):39–43CrossRefPubMed Sheth RD, Abram HS (2010) Absence epilepsy with focal clinical and electrographic seizures. Semin Pediatr Neurol 17(1):39–43CrossRefPubMed
go back to reference Sinclair DB, Unwala H (2007) Absence epilepsy in childhood: electroencephalography (EEG) does not predict outcome. J Child Neurol 22(7):799–802CrossRefPubMed Sinclair DB, Unwala H (2007) Absence epilepsy in childhood: electroencephalography (EEG) does not predict outcome. J Child Neurol 22(7):799–802CrossRefPubMed
go back to reference Stroganova TA, Orekhova EV, Prokofyev AO, Tsetlin MM, Gratchev VV, Morozov AA, Obukhov YV (2012) High-frequency oscillatory response to illusory contour in typically developing boys and boys with autism spectrum disorders. Cortex 48(6):701–717CrossRefPubMed Stroganova TA, Orekhova EV, Prokofyev AO, Tsetlin MM, Gratchev VV, Morozov AA, Obukhov YV (2012) High-frequency oscillatory response to illusory contour in typically developing boys and boys with autism spectrum disorders. Cortex 48(6):701–717CrossRefPubMed
go back to reference Tenney JR, Fujiwara H, Horn PS, Jacobson SE, Glauser TA, Rose DF (2013) Focal corticothalamic sources during generalized absence seizures: a MEG study. Epilepsy Res 106(1–2):113–122CrossRefPubMed Tenney JR, Fujiwara H, Horn PS, Jacobson SE, Glauser TA, Rose DF (2013) Focal corticothalamic sources during generalized absence seizures: a MEG study. Epilepsy Res 106(1–2):113–122CrossRefPubMed
go back to reference Uhlhaas PJ, Pipa G, Neuenschwander S, Wibral M, Singer W (2011) A new look at gamma? High- (>60 Hz) gamma-band activity in cortical networks: function, mechanisms and impairment. Prog Biophys Mol Biol 105(1–2):14–28CrossRefPubMed Uhlhaas PJ, Pipa G, Neuenschwander S, Wibral M, Singer W (2011) A new look at gamma? High- (>60 Hz) gamma-band activity in cortical networks: function, mechanisms and impairment. Prog Biophys Mol Biol 105(1–2):14–28CrossRefPubMed
go back to reference Urrestarazu E, Chander R, Dubeau F, Gotman J (2007) Interictal high-frequency oscillations (100–500 Hz) in the intracerebral EEG of epileptic patients. Brain 130(Pt 9):2354–2366CrossRefPubMed Urrestarazu E, Chander R, Dubeau F, Gotman J (2007) Interictal high-frequency oscillations (100–500 Hz) in the intracerebral EEG of epileptic patients. Brain 130(Pt 9):2354–2366CrossRefPubMed
go back to reference Worrell G, Gotman J (2011) High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med 5(5):557–566PubMedCentralCrossRefPubMed Worrell G, Gotman J (2011) High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med 5(5):557–566PubMedCentralCrossRefPubMed
go back to reference Worrell GA, Jerbi K, Kobayashi K, Lina JM, Zelmann R, Le Van Quyen M (2012) Recording and analysis techniques for high-frequency oscillations. Prog Neurobiol 98(3):265–278PubMedCentralCrossRefPubMed Worrell GA, Jerbi K, Kobayashi K, Lina JM, Zelmann R, Le Van Quyen M (2012) Recording and analysis techniques for high-frequency oscillations. Prog Neurobiol 98(3):265–278PubMedCentralCrossRefPubMed
go back to reference Xiang J, Liu Y, Wang Y, Kirtman EG, Kotecha R, Chen Y, Huo X, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Leach J, Jones B, DeGrauw T, Rose D (2009) Frequency and spatial characteristics of high-frequency neuromagnetic signals in childhood epilepsy. Epileptic Disord 11(2):113–125PubMed Xiang J, Liu Y, Wang Y, Kirtman EG, Kotecha R, Chen Y, Huo X, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Leach J, Jones B, DeGrauw T, Rose D (2009) Frequency and spatial characteristics of high-frequency neuromagnetic signals in childhood epilepsy. Epileptic Disord 11(2):113–125PubMed
go back to reference Xiang J, Wang Y, Chen Y, Liu Y, Kotecha R, Huo X, Rose DF, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Jones B, DeGrauw T (2010) Noninvasive localization of epileptogenic zones with ictal high-frequency neuromagnetic signals. J Neurosurg Pediatr 5(1):113–122CrossRefPubMed Xiang J, Wang Y, Chen Y, Liu Y, Kotecha R, Huo X, Rose DF, Fujiwara H, Hemasilpin N, Lee K, Mangano FT, Jones B, DeGrauw T (2010) Noninvasive localization of epileptogenic zones with ictal high-frequency neuromagnetic signals. J Neurosurg Pediatr 5(1):113–122CrossRefPubMed
go back to reference Xiang J, Luo Q, Kotecha R, Korman A, Zhang F, Luo H, Fujiwara H, Hemasilpin N, Rose DF (2014) Accumulated source imaging of brain activity with both low and high-frequency neuromagnetic signals. Front Neuroinf 8(57):1–17 Xiang J, Luo Q, Kotecha R, Korman A, Zhang F, Luo H, Fujiwara H, Hemasilpin N, Rose DF (2014) Accumulated source imaging of brain activity with both low and high-frequency neuromagnetic signals. Front Neuroinf 8(57):1–17
go back to reference Yao B, Salenius S, Yue GH, Brown RW, Liu JZ (2007) Effects of surface EMG rectification on power and coherence analyses: an EEG and MEG study. J Neurosci Methods 159(2):215–223CrossRefPubMed Yao B, Salenius S, Yue GH, Brown RW, Liu JZ (2007) Effects of surface EMG rectification on power and coherence analyses: an EEG and MEG study. J Neurosci Methods 159(2):215–223CrossRefPubMed
go back to reference Zijlmans M, Jiruska P, Zelmann R, Leijten FS, Jefferys JG, Gotman J (2012) High-frequency oscillations as a new biomarker in epilepsy. Ann Neurol 71(2):169–178PubMedCentralCrossRefPubMed Zijlmans M, Jiruska P, Zelmann R, Leijten FS, Jefferys JG, Gotman J (2012) High-frequency oscillations as a new biomarker in epilepsy. Ann Neurol 71(2):169–178PubMedCentralCrossRefPubMed
Metadata
Title
Quantification of Interictal Neuromagnetic Activity in Absence Epilepsy with Accumulated Source Imaging
Authors
Jing Xiang
Jeffrey R. Tenney
Abraham M. Korman
Kimberly Leiken
Douglas F. Rose
Elana Harris
Weihong Yuan
Paul S. Horn
Katherine Holland
David W. Loring
Tracy A. Glauser
Publication date
01-11-2015
Publisher
Springer US
Published in
Brain Topography / Issue 6/2015
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI
https://doi.org/10.1007/s10548-014-0411-5

Other articles of this Issue 6/2015

Brain Topography 6/2015 Go to the issue