fMRI pp 127-139 | Cite as

Imaging Epileptic Seizures Using fMRI

Abstract

Magnetic resonance imaging (MRI) has had an extraordinary impact on the diagnosis and management of epilepsy. Contemporary high-field strength MRI enables detailed in vivo imaging of lesions that underlie symptomatic epilepsies, for example, hippocampal sclerosis or malformations of cortical development. This routine use of high-field MRI in clinical epilepsy has also contributed to the increasing interest in the potential use of functional MRI (fMRI) to image the abnormal brain function that underlies epilepsy. Here, we give a brief overview of epilepsy, the current state of fMRI for the difficult problem of imaging epileptic seizures, and introduce the topic of neurovascular coupling in the epileptic brain and the constraints this imposes on fMRI interpretation.

Keywords

Status Epilepticus Arterial Spin Label Bold Signal Focal Seizure fMRI Experiment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abreu P, Ribeiro M, Forni A, Pires I, Sousa G (2005) Writing epilepsy: a neurophysiological, neuropsychological and neuroimaging study. Epilepsy Behav 6(3):463–466CrossRefPubMedGoogle Scholar
  2. Adelson PD, Nemoto E, Scheuer M, Painter M, Morgan J, Yonas H (1999) Noninvasive continuous monitoring of cerebral oxygenation periictally using near infrared spectros-copy: a preliminary report. Epilepsia 40:1484–1489CrossRefPubMedGoogle Scholar
  3. Aghakhani Y, Bagshaw AP, Bénar CG, Hawco C, Andermann F, Dubeau F, Gotman J (2004) fMRI activation during spike and wave discharges in idiopathic generalized epilepsy. Brain 127(Pt 5):1127–1144CrossRefPubMedGoogle Scholar
  4. Archer JS, Briellman RS, Abbott DF, Syngeniotis A, Wellard RM, Jackson GD (2003a) Benign epilepsy with centro-temporal spikes: spike triggered fMRI shows somato-sensory cortex activity. Epilepsia 44(2):200–204CrossRefGoogle Scholar
  5. Archer JS, Briellmann RS, Syngeniotis A, Abbott DF, Jackson GD (2003b) Spike-triggered fMRI in reading epilepsy: involvement of left frontal cortex working memory area. Neurology 60(3):415–421Google Scholar
  6. Arthurs OJ, Boniface S (2002) How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci 25(1):27–31CrossRefPubMedGoogle Scholar
  7. Avanzini G, Franceschetti S (2003) Cellular biology of epilepto-genesis. Lancet Neurol (1):33–42Google Scholar
  8. Bahar S, Suh M, Zhao M, Schwartz TH (2006) Intrinsic optical signal imaging of neocortical seizures: the ‘epileptic dip’. Neuroreport 17(5):499–503CrossRefPubMedGoogle Scholar
  9. Baumgartner C, Serles W, Leutmezer F, Pataraia E, Aull S, Czech T, Pietrzyk U, Relic A, Podreka I (1998) Preictal SPECT in temporal lobe epilepsy: regional cerebral blood flow is increased prior to electroencephalography-seizure onset. J Nucl Med 39(6):978–982PubMedGoogle Scholar
  10. Blumenfeld H (2005) Cellular and network mechanisms of spike-wave seizures. Epilepsia 46(Suppl 9):21–33CrossRefPubMedGoogle Scholar
  11. Boor R, Jacobs J, Hinzmann A, Bauermann T, Scherg M, Boor S, Vucurevic G, Pfleiderer C, Kutschke G, Stoeter P (2007) Combined spike-related functional MRI and multiple source analysis in the non-invasive spike localization of benign rolandic epilepsy. Clin Neurophysiol 118(4):901–909CrossRefPubMedGoogle Scholar
  12. Buzsaki G (1991) The thalamic clock: emergent network properties. Neuroscience 41(2–3):351–364CrossRefPubMedGoogle Scholar
  13. Carmichael DW, Hamandi K, Laufs H, Duncan JS, Thomas DL, Lemieux L (2008) An investigation of the relationship between BOLD and perfusion signal changes during epileptic generalised spike wave activity. Magn Reson Imaging 26(7):870–873CrossRefPubMedGoogle Scholar
  14. De Simone R, Silvestrini M, Marciani MG, Curatolo P (1998) Changes in cerebral blood flow velocities during childhood absence seizures. Pediatr Neurol 18:132–135CrossRefPubMedGoogle Scholar
  15. Detre JA, Zhang W, Roberts DA, Silva AC, Williams DS, Grandis DJ, Koretsky AP, Leigh JS (1994) Tissue specific perfusion imaging using arterial spin labeling. NMR Biomed 7(1–2):75–82CrossRefPubMedGoogle Scholar
  16. Detre JA, Sirven JI, Alsop DC, O'Connor MJ, French JA (1995) Localization of subclinical ictal activity by functional magnetic resonance imaging: correlation with invasive monitoring. Ann Neurol 38(4):618–624CrossRefPubMedGoogle Scholar
  17. Di Bonaventura C, CarnfiM, Vaudano AE, Pantano P, Garreffa G, Le Piane E, Maraviglia B, Bozzao L, Manfredi M, Prencipe M, Giallonardo AT (2006) Ictal hemodynamic changes in late-onset rasmussen encephalitis. Ann Neurol 59(2):432–433CrossRefPubMedGoogle Scholar
  18. Diehl B, Knecht S, Deppe M, Young C, Stodieck SR (1998) Cerebral hemodynamic response to generalized spike-wave discharges. Epilepsia 39:1284–1289CrossRefPubMedGoogle Scholar
  19. Dymond AM, Crandall PH (1976) Oxygen availability and blood flow in the temporal lobes during spontaneous epileptic seizures in man. Brain Res 102(1):191–196CrossRefPubMedGoogle Scholar
  20. Elger CE, Lehnertz K (1998) Seizure prediction by non-linear time series analysis of brain electrical activity. Eur J Neurosci 10(2):786–789CrossRefPubMedGoogle Scholar
  21. Espay AJ, Schmithorst VJ, Szaflarski JP (2008) Chronic isolated hemifacial spasm as a manifestation of epilepsia partialis continua. Epilepsy Behav 12(2):332–336CrossRefPubMedGoogle Scholar
  22. Federico P, Abbott DF, Briellmann RS, Harvey AS, Jackson GD (2005) Functional MRI of the pre-ictal state. Brain 128(Pt 8):1811–1817CrossRefPubMedGoogle Scholar
  23. Folbergrová J, Ingvar M, Siesjö BK (1981) Metabolic changes in cerebral cortex, hippocampus, and cerebellum during sustained bicuculline-induced seizures. J Neurochem 37(5):1228–1238CrossRefPubMedGoogle Scholar
  24. Frostig RD, Lieke EE, Ts'o DY, Grinvald A (1990) Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo highresolution optical imaging of intrinsic signals. Proc Natl Acad Sci U S A 87(16):6082–6086CrossRefPubMedGoogle Scholar
  25. Garraux G, Hallett M, Talagala SL (2005) CASL fMRI of subcortico-cortical perfusion changes during memory-guided finger sequences. Neuroimage 25(1):122–132CrossRefPubMedGoogle Scholar
  26. Gloor P. (1968) Generalized cortico-reticular epilepsies. Some considerations on the pathophysiology of generalized bilaterally synchronous spike and wave discharge, Epilepsia 2 pp. 249–263Google Scholar
  27. Gotman J (2008) Epileptic networks studied with EEG-fMRI. Epilepsia 49(Suppl 3):42–51CrossRefPubMedGoogle Scholar
  28. Gotman J, Grova C, Bagshaw A, Kobayashi E, Aghakhani Y, Dubeau F (2005) Generalized epileptic discharges show thal-amocortical activation and suspension of the default state of the brain. Proc Natl Acad Sci U S A 102(42):15236–15240CrossRefPubMedGoogle Scholar
  29. Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 100(1):253–258CrossRefPubMedGoogle Scholar
  30. Hamandi K et al (2006) EEG-fMRI of idiopathic and secondarily generalized epilepsies. Neuroimage 31(4):1700–1710CrossRefPubMedGoogle Scholar
  31. Hamandi K, Laufs H, Nöth U, Carmichael DW, Duncan JS, Lemieux L (2008) BOLD and perfusion changes during epileptic generalised spike wave activity. Neuroimage 39(2):608–618CrossRefPubMedGoogle Scholar
  32. Hauser WA, Hesdorffer DC (1990) Epilepsy: frequency, causes and consequences. Demos Vermande, New YorkGoogle Scholar
  33. Hauser WA, Annegers JF, Kurland LT (1991) Prevalence of epilepsy in Rochester, Minnesota1940–1980. Epilepsia 32:429–445CrossRefPubMedGoogle Scholar
  34. Hawco CS, Bagshaw AP, Lu Y, Dubeau F, Gotman J (2007) BOLD changes occur prior to epileptic spikes seen on scalp EEG. Neuroimage 35(4):1450–1458CrossRefPubMedGoogle Scholar
  35. Hill RA, Chiappa KH, Huang-Hellinger F, Jenkins BG (1999) Hemodynamic and metabolic aspects of photosensitive epilepsy revealed by functional magnetic resonance imaging and magnetic resonance spectroscopy. Epilepsia 40(7):912–920CrossRefPubMedGoogle Scholar
  36. Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999) Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc Natl Acad Sci U S A 96(16):9403–9408CrossRefPubMedGoogle Scholar
  37. Hoshi Y, Tamura M (1992) Cerebral oxygenation state in chemically induced seizures in the rat,Äîstudy by near infrared spectrophotometry. Adv Exp Med Biol 316:137–142PubMedGoogle Scholar
  38. Hwang DY, Golby AJ (2006) The brain basis for episodic memory: insights from functional MRI, intracranial EEG, and patients with epilepsy. Epilepsy Behav 8(1):115–126CrossRefPubMedGoogle Scholar
  39. Jackson GD, Connelly A, Cross JH, Gordon I, Gadian DG (1994) Functional magnetic resonance imaging of focal seizures. Neurology 44(5):850–856PubMedGoogle Scholar
  40. Jacobs J, Hawco C, Kobayashi E, Boor R, LeVan P, Stephani U, Siniatchkin M, Gotman J (2008) Variability of the hemody-namic response as a function of age and frequency of epileptic discharge in children with epilepsy. Neuroimage 40(2):601–614CrossRefPubMedGoogle Scholar
  41. Kobayashi E, Hawco CS, Grova C, Dubeau F, Gotman J (2006) Widespread and intense BOLD changes during brief focal electrographic seizures. Neurology 66(7):1049–1055CrossRefPubMedGoogle Scholar
  42. Krings T, Töpper R, Reinges MH, Foltys H, Spetzger U, Chiappa KH, Gilsbach JM, Thron A (2000) Hemodynamic changes in simple partial epilepsy: a functional MRI study. Neurology 54(2):524–527PubMedGoogle Scholar
  43. Kurtzke JF (1982) The current neurologic burden of illness and injury in the United States. Neurology 32(11):1207–1214PubMedGoogle Scholar
  44. Laufs H, Duncan JS (2007) Electroencephalography/functional MRI in human epilepsy: what it currently can and cannot do. Curr Opin Neurol 20(4):417–423CrossRefPubMedGoogle Scholar
  45. Laufs H, Lengler U, Hamandi K, Kleinschmidt A, Krakow K (2006) Linking generalized spike-and-wave discharges and resting state brain activity by using EEG/fMRI in a patient with absence seizures. Epilepsia 47(2):444–448CrossRefPubMedGoogle Scholar
  46. Laurienti PJ (2004) Deactivations, global signal, and the default mode of brain function. J Cogn Neurosci 16(9):1481–1483. No abstract availableCrossRefPubMedGoogle Scholar
  47. Lazeyras F, Blanke O, Zimine I, Delavelle J, Perrig SH, Seeck M (2000) MRI, (1)H-MRS, and functional MRI during and after prolonged nonconvulsive seizure activity. Neurology 55(11):1677–1682PubMedGoogle Scholar
  48. Leal A, Dias A, Vieira JP, Secca M, Jordã o C (2006) The BOLD effect of interictal spike activity in childhood occipital lobe epilepsy. Epilepsia 47(9):1536–1542CrossRefPubMedGoogle Scholar
  49. Lehnertz K, Elger CE (1995) Spatio-temporal dynamics of the primary epileptogenic area in temporal lobe epilepsy characterized by neuronal complexity loss. Electroencephalogr Clin Neurophysiol 95(2):108–117CrossRefPubMedGoogle Scholar
  50. Lemieux L, Salek-Haddadi A, Lund TE, Laufs H, Carmichael D (2007) Modelling large motion events in fMRI studies of patients with epilepsy. Magn Reson Imaging 25(6):894–901CrossRefPubMedGoogle Scholar
  51. Lengler U, Kafadar I, Neubauer BA, Krakow K (2007) fMRI correlates of interictal epileptic activity in patients with idio-pathic benign focal epilepsy of childhood. A simultaneous EEG-functional MRI study. Epilepsy Res 75(1):29–38CrossRefPubMedGoogle Scholar
  52. Litt B, Esteller R, Echauz J, D'Alessandro M, Shor R, Henry T, Pennell P, Epstein C, Bakay R, Dichter M, Vachtsevanos G (2001) Epileptic seizures may begin hours in advance of clinical onset: a report of five patients. Neuron 30(1):51–64CrossRefPubMedGoogle Scholar
  53. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412(6843):150–157CrossRefPubMedGoogle Scholar
  54. Makiranta M, Ruohonen J, Suominen K, Niinimaki J, Sonkajarvi E, Kiviniemi V, Seppanen T, Alahuhta S, Jantti V, Tervonen O (2005) BOLD signal increase preceeds EEG spike activity, a dynamic penicillin induced focal epilepsy in deep anesthesia. Neuroimage 27:715–724CrossRefPubMedGoogle Scholar
  55. Mazoyer B, Zago L, Mellet E, Bricogne S, Etard O Houdé O, Crivello F, Joliot M, Petit L, Tzourio-Mazoyer N (2001) Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res Bull 54(3):287–298CrossRefPubMedGoogle Scholar
  56. McCormick DA, Contreras D (2001) On the cellular and network bases of epileptic seizures. Annu Rev Physiol 63:815–846CrossRefPubMedGoogle Scholar
  57. Meeren H, van Luijtelaar G, Lopes da Silva F, Coenen A (2005) Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. Arch Neurol 62(3):371–376CrossRefPubMedGoogle Scholar
  58. Moeller F et al (2008) Changes in activity of striato-thalamo-cortical network precede generalized spike wave discharges. Neuroimage 39(4):839–1849CrossRefGoogle Scholar
  59. Morocz IA, Karni A, Haut S, Lantos G, Liu G (2003) fMRI of triggerable aurae in musicogenic epilepsy. Neurology 60(4):705–709PubMedGoogle Scholar
  60. Neuroimaging Subcommission of the ILAE (2000) Commission on Diagnostic Strategies recommendations for functional neuroimaging of persons with epilepsy. Epilepsia 41(10):1350–1356CrossRefGoogle Scholar
  61. Penfield W (1933) The evidence for a cerebral vascular mechanism in epilepsy. Ann Internal Med vol 7(3):303–310Google Scholar
  62. Penfield W and Jasper H. (1954) Epilepsy and the functional anatomy of the human brain. Boston: Little, Brown & Co., 896 ppGoogle Scholar
  63. Polack PO, Guillemain I, Hu E, Deransart C, Depaulis A, Charpier S (2007) Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures. J Neurosci 27(24):6590–6599CrossRefPubMedGoogle Scholar
  64. Raichle ME (2003) Functional brain imaging and human brain function. J Neurosci 23(10):3959–3962PubMedGoogle Scholar
  65. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GLA (2001) default mode of brain function. Proc Natl Acad Sci U S A 98(2):676–682CrossRefPubMedGoogle Scholar
  66. Salek-Haddadi A, Merschhemke M, Lemieux L, Fish DR (2002) Simultaneous EEG-Correlated Ictal fMRI. Neuroimage 16(1):32–40CrossRefPubMedGoogle Scholar
  67. Salek-Haddadi A, Lemieux L, Merschhemke M, Friston KJ, Duncan JS, Fish DR (2003). Functional magnetic resonance imaging of human absence seizures. Ann Neurol. 53(5):663–7CrossRefPubMedGoogle Scholar
  68. Sander JW (2003) The epidemiology of epilepsy revisited. Curr Opin Neurol 16:165–170CrossRefPubMedGoogle Scholar
  69. Schwartz TH (2007) Neurovascular coupling and epilepsy: hemodynamic markers for localizing and predicting seizure onset. Epilepsy Curr 7(4):91–94CrossRefPubMedGoogle Scholar
  70. Senanayake N (1987). Epileptic seizures evoked by the Rubik's cube. J Neurol Neurosurg Psychiatry. 50(11):1553–4CrossRefPubMedGoogle Scholar
  71. Shariff S, Suh M, Zhao M, Ma H, Schwartz TH (2006) Recent developments in oximetry and perfusion-based mapping techniques and their role in the surgical treatment of neocor-tical epilepsy. Epilepsy Behav 8(2):363–375CrossRefPubMedGoogle Scholar
  72. Spencer SS (2002) Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 43(3):219–227CrossRefPubMedGoogle Scholar
  73. Stefanovic B, Warnking JM, Kobayashi E, Bagshaw AP, Hawco C, Dubeau F, Gotman J, Pike GB (2005) Hemodynamic and metabolic responses to activation, deactivation and epileptic discharges. Neuroimage 28(1):205–215CrossRefPubMedGoogle Scholar
  74. Suh M, Bahar S, Mehta AD, Schwartz TH (2006a) Blood volume and hemoglobin oxygenation response following electrical stimulation of human cortex. Neuroimage 31(1):66–75CrossRefGoogle Scholar
  75. Suh M, Ma H, Zhao M, Sharif S, Schwartz TH (2006b) Neurovascular coupling and oximetry during epileptic events. Mol Neurobiol 33(3):181–197CrossRefGoogle Scholar
  76. Swanson SJ, Sabsevitz DS, Hammeke TA, Binder JR (2007) Functional magnetic resonance imaging of language in epilepsy. Neuropsychol Rev 17(4):491–504CrossRefPubMedGoogle Scholar
  77. Tenney JR, Marshall PC, King JA, Ferris CF (2004) fMRI of generalized absence status epilepticus in conscious marmoset monkeys reveals corticothalamic activation. Epilepsia 45(10):1240–1247CrossRefPubMedGoogle Scholar
  78. Weinand ME, Carter LP, Patton DD, Oommen KJ, Labiner DM, Talwar D (1994) Long-term surface cortical cerebral blood flow monitoring in temporal lobe epilepsy. Neurosurgery 35:657–664CrossRefPubMedGoogle Scholar
  79. Weinand ME, Carter LP, el-Saadany WF, Sioutos PJ, Labiner DM, Oommen KJ (1997) Cerebral blood flow and temporal lobe epileptogenicity. J Neurosurg 86(2):226–232CrossRefPubMedGoogle Scholar
  80. Wiebe S, Blume WT, Girvin JP et al (2001) A randomized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345:311–318CrossRefPubMedGoogle Scholar
  81. Wolf RL, Alsop DC, Levy-Reis I, Meyer PT, Maldjian JA, Gonzalez-Atavales J, French JA, Alavi A, Detre JA (2001) Detection of mesial temporal lobe hypoperfusion in patients with temporal lobe epilepsy by use of arterial spin labeled perfusion MR imaging. AJNR Am J Neuroradiol 22(7):1334–1341PubMedGoogle Scholar
  82. Wu R, Bruening R, Noachtar S, et al (1999) MR measurement of regional relative cerebral blood volume in epilepsy. J Magn Reson Imaging 9:435–440CrossRefPubMedGoogle Scholar
  83. Yeo DT, Fessler JA, Kim B (2008) Motion robust magnetic susceptibility and field inhomogeneity estimation using regularized image restoration techniques for fMRI. Med Image Comput Comput Assist Interv Int Conf Med Image Comput Comput Assist Interv 11(Pt 1):991–998Google Scholar
  84. Zyss J, Xie-Brustolin J, Ryvlin P, Peysson S, Beschet A, Sappey-Marinier D, Hermier M, Thobois S (2007) Epilepsia partialis continua with dystonic hand movement in a patient with a malformation of cortical development. Mov Disord 22(12):1793–1796CrossRefPubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.The Mahoney Institute of Neurological SciencesUniversity of PennsylvaniaPhiladelphiaUSA

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