Download PDF
Journal of Pediatric Epilepsy 2015; 04(04): 174-183
DOI: 10.1055/s-0035-1559812
Review Article
Georg Thieme Verlag KG Stuttgart · New York

Simultaneous Electroencephalography and Functional Magnetic Resonance Imaging and the Identification of Epileptic Networks in Children

Thomas C. Maloney
1   Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States
,
Jeffrey R. Tenney
1   Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States
,
Jerzy P. Szaflarski
2   University of Alabama at Birmingham, Birmingham, Alabama, United States
,
Jennifer Vannest
1   Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, United States
› Author Affiliations
Further Information

Publication History

03 July 2014

04 December 2014

Publication Date:
18 August 2015 (online)

    Permissions and Reprints

Abstract

Electroencephalography and functional magnetic resonance imaging (EEG/fMRI) takes advantage of the high temporal resolution of EEG in combination with the high spatial resolution of fMRI. These features make it particularly applicable to the study of epilepsy in which the event duration (e.g., interictal epileptiform discharges) is short, typically less than 200 ms. Interictal or ictal discharges can be identified on EEG and be used for source localization in fMRI analyses. The acquisition of simultaneous EEG/fMRI involves the use of specialized EEG hardware that is safe in the MR environment and comfortable to the participant. Advanced data analysis approaches such as independent component analysis conducted alone or sometimes combined with others, for example, Granger causality or “sliding window” analyses are currently thought to be most appropriate for EEG/fMRI data. These approaches make it possible to identify networks of brain regions associated with ictal and/or interictal events allowing examination of the mechanisms critical for generation and propagation through these networks. After initial evaluation in adults, EEG/fMRI has been applied to the examination of the pediatric epilepsy syndromes, including childhood absence epilepsy, benign epilepsy with centrotemporal spikes, Dravet syndrome, and Lennox–Gastaut syndrome. Results of EEG/fMRI studies suggest that the hemodynamic response measured by fMRI may have a different shape in response to epileptic events compared with the response to external stimuli; this may be especially true in the developing brain. Thus, the main goal of this review is to provide an overview of the pediatric applications of EEG/fMRI and its associated findings up until this point.

Keywords

electroencephalogram - functional magnetic resonance imaging - epilepsy
 

  • References

  • 1 Ives JR, Warach S, Schmitt F, Edelman RR, Schomer DL. Monitoring the patient's EEG during echo planar MRI. Electroencephalogr Clin Neurophysiol 1993; 87 (6) 417-420
    CrossrefPubMedGoogle Scholar
  • 2 Allen PJ, Josephs O, Turner R. A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 2000; 12 (2) 230-239
    CrossrefPubMedGoogle Scholar
  • 3 Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L. Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 1998; 8 (3) 229-239
    CrossrefPubMedGoogle Scholar
  • 4 Bénar C, Aghakhani Y, Wang Y , et al. Quality of EEG in simultaneous EEG-fMRI for epilepsy. Clin Neurophysiol 2003; 114 (3) 569-580
    CrossrefPubMedGoogle Scholar
  • 5 Vanderperren K, De Vos M, Ramautar JR , et al. Removal of BCG artifacts from EEG recordings inside the MR scanner: a comparison of methodological and validation-related aspects. Neuroimage 2010; 50 (3) 920-934
    CrossrefPubMedGoogle Scholar
  • 6 Holland SK, Byars AW, Plante E, Szaflarski JP, Dietrich K, Altaye M. Studies support probable long-term safety of MRI. Science 2010; 329 (5991) 512-513
    PubMedGoogle Scholar
  • 7 Holland SK, Altaye M, Robertson S, Byars AW, Plante E, Szaflarski JP. Data on the safety of repeated MRI in healthy children. Neuroimage Clin 2014; 4: 526-530
    CrossrefPubMedGoogle Scholar
  • 8 Altaye M, Holland SK, Wilke M, Gaser C. Infant brain probability templates for MRI segmentation and normalization. Neuroimage 2008; 43 (4) 721-730
    CrossrefPubMedGoogle Scholar
  • 9 Wilke M, Holland SK, Altaye M, Gaser C. Template-O-Matic: a toolbox for creating customized pediatric templates. Neuroimage 2008; 41 (3) 903-913
    CrossrefPubMedGoogle Scholar
  • 10 Ben-Ari Y. Basic developmental rules and their implications for epilepsy in the immature brain. Epileptic Disord 2006; 8 (2) 91-102
    PubMedGoogle Scholar
  • 11 Byars AW, Holland SK, Strawsburg RH , et al. Practical aspects of conducting large-scale functional magnetic resonance imaging studies in children. J Child Neurol 2002; 17 (12) 885-890
    CrossrefPubMedGoogle Scholar
  • 12 Vannest J, Szaflarski JP, Eaton KP , et al. Functional magnetic resonance imaging reveals changes in language localization in children with benign childhood epilepsy with centrotemporal spikes. J Child Neurol 2013; 28 (4) 435-445
    CrossrefPubMedGoogle Scholar
  • 13 Masamoto K, Kanno I. Anesthesia and the quantitative evaluation of neurovascular coupling. J Cereb Blood Flow Metab 2012; 32 (7) 1233-1247
    CrossrefPubMedGoogle Scholar
  • 14 Patel AM, Cahill LD, Ret J, Schmithorst V, Choo D, Holland S. Functional magnetic resonance imaging of hearing-impaired children under sedation before cochlear implantation. Arch Otolaryngol Head Neck Surg 2007; 133 (7) 677-683
    CrossrefPubMedGoogle Scholar
  • 15 Robertson S, Karunananayaka P, Arjmand E , et al. Eds. fMRI of Infants for Cochlear Implant Staging is Influenced by Sedation. Poster presented at: Proceedings of the Society for Ear, Nose and Throat Advances in Children; December 3–5, 2010; Cincinnati, OH
    PubMedGoogle Scholar
  • 16 Boor R, Jacobs J, Hinzmann A , et al. Combined spike-related functional MRI and multiple source analysis in the non-invasive spike localization of benign rolandic epilepsy. Clin Neurophysiol 2007; 118 (4) 901-909
    CrossrefPubMedGoogle Scholar
  • 17 Patel MR, Blum A, Pearlman JD , et al. Echo-planar functional MR imaging of epilepsy with concurrent EEG monitoring. AJNR Am J Neuroradiol 1999; 20 (10) 1916-1919
    PubMedGoogle Scholar
  • 18 Lagerlund TD, Sharbrough FW, Busacker NE. Spatial filtering of multichannel electroencephalographic recordings through principal component analysis by singular value decomposition. J Clin Neurophysiol 1997; 14 (1) 73-82
    CrossrefPubMedGoogle Scholar
  • 19 Kay BP, DiFrancesco MW, Privitera MD, Gotman J, Holland SK, Szaflarski JP. Reduced default mode network connectivity in treatment-resistant idiopathic generalized epilepsy. Epilepsia 2013; 54 (3) 461-470
    CrossrefPubMedGoogle Scholar
  • 20 Stern JM. Simultaneous electroencephalography and functional magnetic resonance imaging applied to epilepsy. Epilepsy Behav 2006; 8 (4) 683-692
    CrossrefPubMedGoogle Scholar
  • 21 Smith SM, Jenkinson M, Woolrich MW , et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23 (Suppl. 01) S208-S219
    CrossrefPubMedGoogle Scholar
  • 22 Friston KJ, Frith CD, Turner R, Frackowiak RS. Characterizing evoked hemodynamics with fMRI. Neuroimage 1995; 2 (2) 157-165
    CrossrefPubMedGoogle Scholar
  • 23 Hawco CS, Bagshaw AP, Lu Y, Dubeau F, Gotman J. BOLD changes occur prior to epileptic spikes seen on scalp EEG. Neuroimage 2007; 35 (4) 1450-1458
    CrossrefPubMedGoogle Scholar
  • 24 Benuzzi F, Mirandola L, Pugnaghi M , et al. Increased cortical BOLD signal anticipates generalized spike and wave discharges in adolescents and adults with idiopathic generalized epilepsies. Epilepsia 2012; 53 (4) 622-630
    CrossrefPubMedGoogle Scholar
  • 25 Szaflarski JP, DiFrancesco M, Hirschauer T , et al. Cortical and subcortical contributions to absence seizure onset examined with EEG/fMRI. Epilepsy Behav 2010; 18 (4) 404-413
    CrossrefPubMedGoogle Scholar
  • 26 de Munck JC, Gonçalves SI, Huijboom L , et al. The hemodynamic response of the alpha rhythm: an EEG/fMRI study. Neuroimage 2007; 35 (3) 1142-1151
    CrossrefPubMedGoogle Scholar
  • 27 Szaflarski JP, Kay B, Gotman J, Privitera MD, Holland SK. The relationship between the localization of the generalized spike and wave discharge generators and the response to valproate. Epilepsia 2013; 54 (3) 471-480
    CrossrefPubMedGoogle Scholar
  • 28 Henson RNA. Analysis of fMRI time series. In: Frackowiak RSJ, Friston KJ, Frith C, . ed. Human Brain Function. 2nd ed. San Francisco, CA: Academic Press; 2003
    Google Scholar
  • 29 Bai X, Vestal M, Berman R , et al. Dynamic time course of typical childhood absence seizures: EEG, behavior, and functional magnetic resonance imaging. J Neurosci 2010; 30 (17) 5884-5893
    CrossrefPubMedGoogle Scholar
  • 30 Carney PW, Masterton RA, Flanagan D, Berkovic SF, Jackson GD. The frontal lobe in absence epilepsy: EEG-fMRI findings. Neurology 2012; 78 (15) 1157-1165
    CrossrefPubMedGoogle Scholar
  • 31 Moeller F, Siebner HR, Wolff S , et al. Changes in activity of striato-thalamo-cortical network precede generalized spike wave discharges. Neuroimage 2008; 39 (4) 1839-1849
    CrossrefPubMedGoogle Scholar
  • 32 Moeller F, Siebner HR, Ahlgrimm N , et al. fMRI activation during spike and wave discharges evoked by photic stimulation. Neuroimage 2009; 48 (4) 682-695
    CrossrefPubMedGoogle Scholar
  • 33 Masterton RA, Jackson GD, Abbott DF. Mapping brain activity using event-related independent components analysis (eICA): specific advantages for EEG-fMRI. Neuroimage 2013; 70: 164-174
    CrossrefPubMedGoogle Scholar
  • 34 Holmes GL. Rolandic epilepsy: clinical and electroencephalographic features. Epilepsy Res Suppl 1992; 6: 29-43
    PubMedGoogle Scholar
  • 35 Lerman P, Kivity S. Benign focal epilepsy of childhood. A follow-up study of 100 recovered patients. Arch Neurol 1975; 32 (4) 261-264
    CrossrefPubMedGoogle Scholar
  • 36 Ma CK, Chan KY. Benign childhood epilepsy with centrotemporal spikes: a study of 50 Chinese children. Brain Dev 2003; 25 (6) 390-395
    CrossrefPubMedGoogle Scholar
  • 37 Clemens B, Majoros E. Sleep studies in benign epilepsy of childhood with rolandic spikes. II. Analysis of discharge frequency and its relation to sleep dynamics. Epilepsia 1987; 28 (1) 24-27
    CrossrefPubMedGoogle Scholar
  • 38 Clemens B, Oláh R. Sleep studies in benign epilepsy of childhood with rolandic spikes. I. Sleep pathology. Epilepsia 1987; 28 (1) 20-23
    CrossrefPubMedGoogle Scholar
  • 39 Blom S, Brorson LO. Central spikes or sharp waves (Rolandic spikes) in children's EEG and their clinical significance. Acta Paediatr Scand 1966; 55 (4) 385-393
    CrossrefPubMedGoogle Scholar
  • 40 Blom S, Heijbel J. Benign epilepsy of children with centro-temporal EEG foci. Discharge rate during sleep. Epilepsia 1975; 16 (1) 133-140
    CrossrefPubMedGoogle Scholar
  • 41 Loiseau P, Beaussart M. The seizures of benign childhood epilepsy with Rolandic paroxysmal discharges. Epilepsia 1973; 14 (4) 381-389
    CrossrefPubMedGoogle Scholar
  • 42 Baumgartner C, Graf M, Doppelbauer A , et al. The functional organization of the interictal spike complex in benign rolandic epilepsy. Epilepsia 1996; 37 (12) 1164-1174
    CrossrefPubMedGoogle Scholar
  • 43 Kamada K, Möller M, Saguer M , et al. Localization analysis of neuronal activities in benign rolandic epilepsy using magnetoencephalography. J Neurol Sci 1998; 154 (2) 164-172
    CrossrefPubMedGoogle Scholar
  • 44 van der Meij W, Wieneke GH, van Huffelen AC. Dipole source analysis of rolandic spikes in benign rolandic epilepsy and other clinical syndromes. Brain Topogr 1993; 5 (3) 203-213
    CrossrefPubMedGoogle Scholar
  • 45 Masterton RA, Harvey AS, Archer JS , et al. Focal epileptiform spikes do not show a canonical BOLD response in patients with benign rolandic epilepsy (BECTS). Neuroimage 2010; 51 (1) 252-260
    CrossrefPubMedGoogle Scholar
  • 46 Lillywhite LM, Saling MM, Harvey AS , et al. Neuropsychological and functional MRI studies provide converging evidence of anterior language dysfunction in BECTS. Epilepsia 2009; 50 (10) 2276-2284
    CrossrefPubMedGoogle Scholar
  • 47 Northcott E, Connolly AM, Berroya A , et al. The neuropsychological and language profile of children with benign rolandic epilepsy. Epilepsia 2005; 46 (6) 924-930
    CrossrefPubMedGoogle Scholar
  • 48 Overvliet GM, Aldenkamp AP, Klinkenberg S , et al. Correlation between language impairment and problems in motor development in children with rolandic epilepsy. Epilepsy Behav 2011; 22 (3) 527-531
    CrossrefPubMedGoogle Scholar
  • 49 Tyvaert L, Hawco C, Kobayashi E, LeVan P, Dubeau F, Gotman J. Different structures involved during ictal and interictal epileptic activity in malformations of cortical development: an EEG-fMRI study. Brain 2008; 131 (Pt 8) 2042-2060
    CrossrefPubMedGoogle Scholar
  • 50 Federico P, Archer JS, Abbott DF, Jackson GD. Cortical/subcortical BOLD changes associated with epileptic discharges: an EEG-fMRI study at 3 T. Neurology 2005; 64 (7) 1125-1130
    CrossrefPubMedGoogle Scholar
  • 51 Thornton R, Vulliemoz S, Rodionov R , et al. Epileptic networks in focal cortical dysplasia revealed using electroencephalography-functional magnetic resonance imaging. Ann Neurol 2011; 70 (5) 822-837
    CrossrefPubMedGoogle Scholar
  • 52 Jacobs J, Rohr A, Moeller F , et al. Evaluation of epileptogenic networks in children with tuberous sclerosis complex using EEG-fMRI. Epilepsia 2008; 49 (5) 816-825
    CrossrefPubMedGoogle Scholar
  • 53 Penry JK, Dreifuss FE. Automatisms associated with the absence of petit mal epilepsy. Arch Neurol 1969; 21 (2) 142-149
    CrossrefPubMedGoogle Scholar
  • 54 Berg AT, Shinnar S, Levy SR , et al. Two-year remission and subsequent relapse in children with newly diagnosed epilepsy. Epilepsia 2001; 42 (12) 1553-1562
    CrossrefPubMedGoogle Scholar
  • 55 Fois A, Malandrini F, Mostardini R. Clinical experiences of petit mal. Brain Dev 1987; 9 (1) 54-59
    CrossrefPubMedGoogle Scholar
  • 56 Trinka E, Baumgartner S, Unterberger I , et al. Long-term prognosis for childhood and juvenile absence epilepsy. J Neurol 2004; 251 (10) 1235-1241
    CrossrefPubMedGoogle Scholar
  • 57 Moeller F, Siebner HR, Wolff S , et al. Simultaneous EEG-fMRI in drug-naive children with newly diagnosed absence epilepsy. Epilepsia 2008; 49 (9) 1510-1519
    CrossrefPubMedGoogle Scholar
  • 58 Gotman J, Grova C, Bagshaw A, Kobayashi E, Aghakhani Y, Dubeau F. Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. Proc Natl Acad Sci U S A 2005; 102 (42) 15236-15240
    CrossrefPubMedGoogle Scholar
  • 59 Carney PW, Masterton RA, Harvey AS, Scheffer IE, Berkovic SF, Jackson GD. The core network in absence epilepsy. Differences in cortical and thalamic BOLD response. Neurology 2010; 75 (10) 904-911
    CrossrefPubMedGoogle Scholar
  • 60 Kay B, Szaflarski JP. EEG/fMRI contributions to our understanding of genetic generalized epilepsies. Epilepsy Behav 2014; 34: 129-135
    CrossrefPubMedGoogle Scholar
  • 61 Masterton RA, Carney PW, Abbott DF, Jackson GD. Absence epilepsy subnetworks revealed by event-related independent components analysis of functional magnetic resonance imaging. Epilepsia 2013; 54 (5) 801-808
    CrossrefPubMedGoogle Scholar
  • 62 Szaflarski JP, Lindsell CJ, Zakaria T, Banks C, Privitera MD. Seizure control in patients with idiopathic generalized epilepsies: EEG determinants of medication response. Epilepsy Behav 2010; 17 (4) 525-530
    CrossrefPubMedGoogle Scholar
  • 63 Aghakhani Y, Bagshaw AP, Bénar CG , et al. fMRI activation during spike and wave discharges in idiopathic generalized epilepsy. Brain 2004; 127 (Pt 5) 1127-1144
    CrossrefPubMedGoogle Scholar
  • 64 Szaflarski JP, Allendorfer JB. Topiramate and its effect on fMRI of language in patients with right or left temporal lobe epilepsy. Epilepsy Behav 2012; 24 (1) 74-80
    CrossrefPubMedGoogle Scholar
  • 65 Yasuda CL, Centeno M, Vollmar C , et al. The effect of topiramate on cognitive fMRI. Epilepsy Res 2013; 105 (1-2) 250-255
    CrossrefPubMedGoogle Scholar
  • 66 Kay BP, Holland SK, Privitera MD, Szaflarski JP. Differences in paracingulate connectivity associated with epileptiform discharges and uncontrolled seizures in genetic generalized epilepsy. Epilepsia 2014; 55 (2) 256-263
    CrossrefPubMedGoogle Scholar
  • 67 Siniatchkin M, Coropceanu D, Moeller F, Boor R, Stephani U. EEG-fMRI reveals activation of brainstem and thalamus in patients with Lennox-Gastaut syndrome. Epilepsia 2011; 52 (4) 766-774
    CrossrefPubMedGoogle Scholar
  • 68 Pillay N, Archer JS, Badawy RA, Flanagan DF, Berkovic SF, Jackson G. Networks underlying paroxysmal fast activity and slow spike and wave in Lennox-Gastaut syndrome. Neurology 2013; 81 (7) 665-673
    CrossrefPubMedGoogle Scholar
  • 69 Moeller F, Groening K, Moehring J , et al. EEG-fMRI in myoclonic astatic epilepsy (Doose syndrome). Neurology 2014; 82 (17) 1508-1513
    CrossrefPubMedGoogle Scholar