Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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):950–962

    Article  PubMed  Google Scholar 

  • 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):1960–1967

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):1017–1023

    Article  PubMed  Google Scholar 

  • 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):1454–1465

    Article  PubMed  Google Scholar 

  • 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):393–400

    PubMed  Google Scholar 

  • Ebersole JS, Ebersole SM (2010) Combining MEG and EEG source modeling in epilepsy evaluations. J Clin Neurophysiol 27(6):360–371

    Article  PubMed  Google Scholar 

  • Engel J Jr, da Silva FL (2012) High-frequency oscillations—where we are and where we need to go. Prog Neurobiol 98(3):316–318

    Article  PubMed Central  PubMed  Google Scholar 

  • Engel J Jr, Bragin A, Staba R, Mody I (2009) High-frequency oscillations: what is normal and what is not? Epilepsia 50(4):598–604

    Article  PubMed  Google Scholar 

  • 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):389–399

    Article  Google Scholar 

  • 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 240–231

    Article  PubMed  Google Scholar 

  • 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):790–799

    Article  Google Scholar 

  • Gotman J (2010) High frequency oscillations: the new EEG frontier? Epilepsia 51(Suppl 1):63–65

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):848–857

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):1213–1226

    Article  CAS  PubMed  Google Scholar 

  • 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 193:145–162

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):302–315

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

  • 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):2209–2217

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):540–548

    Article  Google Scholar 

  • Mariani E, Rossi LN, Vajani S (2011) Interictal paroxysmal EEG abnormalities in childhood absence epilepsy. Seizure 20(4):299–304

    Article  PubMed  Google Scholar 

  • 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):308–317

    Article  PubMed  Google Scholar 

  • 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 566:21–26

    Article  CAS  PubMed  Google Scholar 

  • 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):2000–2010

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):432–440

    Article  CAS  PubMed  Google Scholar 

  • Ogura K, Maegaki Y, Koeda T (2005) EEG evaluation of fixation-off sensitivity in eyelid myoclonia with absences. Pediatr Neurol 33(2):142–145

    Article  PubMed  Google Scholar 

  • 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):197–204

    Article  CAS  PubMed  Google Scholar 

  • Rampp S, Stefan H (2007) Magnetoencephalography in presurgical epilepsy diagnosis. Expert Rev Med Devices 4(3):335–347

    Article  PubMed  Google Scholar 

  • Richardson MP (2011) New observations may inform seizure models: very fast and very slow oscillations. Prog Biophys Mol Biol 105(1–2):5–13

    Article  PubMed  Google Scholar 

  • Schubert R (2005) Attention deficit disorder and epilepsy. Pediatr Neurol 32(1):1–10

    Article  PubMed  Google Scholar 

  • Sheth RD, Abram HS (2010) Absence epilepsy with focal clinical and electrographic seizures. Semin Pediatr Neurol 17(1):39–43

    Article  PubMed  Google Scholar 

  • Sinclair DB, Unwala H (2007) Absence epilepsy in childhood: electroencephalography (EEG) does not predict outcome. J Child Neurol 22(7):799–802

    Article  PubMed  Google Scholar 

  • Sohal VS (2012) Insights into cortical oscillations arising from optogenetic studies. Biol Psychiatry 71(12):1039–1045

    Article  PubMed Central  PubMed  Google Scholar 

  • Stacey WC, Krieger A, Litt B (2011) Network recruitment to coherent oscillations in a hippocampal computer model. J Neurophysiol 105(4):1464–1481

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):701–717

    Article  PubMed  Google Scholar 

  • 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):113–122

    Article  PubMed  Google Scholar 

  • 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):14–28

    Article  PubMed  Google Scholar 

  • 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):2354–2366

    Article  PubMed  Google Scholar 

  • Vrba J, Robinson SE (2001) Signal processing in magnetoencephalography. Methods 25(2):249–271

    Article  CAS  PubMed  Google Scholar 

  • Wood H (2011) High-frequency oscillations pinpoint the seizure-onset zone. Nat Rev Neurol 7(9):475

    Article  PubMed  Google Scholar 

  • Worrell G, Gotman J (2011) High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med 5(5):557–566

    Article  PubMed Central  PubMed  Google Scholar 

  • 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):265–278

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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):113–125

    PubMed  Google Scholar 

  • 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):113–122

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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):215–223

    Article  PubMed  Google Scholar 

  • 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):169–178

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partially supported by a Trustee Grant from Cincinnati Children’s Hospital Medical Center and Grant Number R21NS072817 from the National Institute of Neurological Disorders and Stroke (NINDS), the National Institutes of Health. Portions of this study were funded by a “Taking Flight” award from the Citizens United for Research in Epilepsy (CURE) (J.R.T.). We thank Ms. Hisako Fujiwara and Dr. Nat Hemasilpin for helping with MEG data acquisition. We thank all participants and their families for their time and support.

Conflict of interest

The authors have declared that no competing interests exist.

Author information

Authors and Affiliations

  1. MEG Center, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Jing Xiang, Jeffrey R. Tenney, Abraham M. Korman, Kimberly Leiken & Douglas F. Rose

  2. Division of Neurology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave, Cincinnati, OH, 45229, USA

    Jing Xiang, Jeffrey R. Tenney, Douglas F. Rose, Paul S. Horn, Katherine Holland & Tracy A. Glauser

  3. Child & Adolescent Psychiatry, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Elana Harris

  4. Department of Radiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Weihong Yuan

  5. Departments of Neurology and Pediatrics, Emory University School of Medicine, Atlanta, GA, USA

    David W. Loring

  6. Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Paul S. Horn

Authors
  1. Jing Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey R. Tenney
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abraham M. Korman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kimberly Leiken
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Douglas F. Rose
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elana Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Weihong Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paul S. Horn
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Katherine Holland
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. David W. Loring
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Tracy A. Glauser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeffrey R. Tenney.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiang, J., Tenney, J.R., Korman, A.M. et al. Quantification of Interictal Neuromagnetic Activity in Absence Epilepsy with Accumulated Source Imaging. Brain Topogr 28, 904–914 (2015). https://doi.org/10.1007/s10548-014-0411-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-014-0411-5

Keywords

Search

Navigation