Widespread grey matter changes and hemodynamic correlates to interictal epileptiform discharges in pharmacoresistant mesial temporal epilepsy

Journal of Neurology

Volumn 260, Issue 6, 2013, Pages 1601-1610

  Wiest, Roland ^a   Estermann, Lea ^a   Scheidegger, Olivier ^a   Rummel, Christian ^a   Jann, Kay ^a   Seeck, Margitta ^b   Schindler, Kaspar ^a   Hauf, Martinus ^a,c  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c Bethesda Epilepsy Clinic   (Switzerland)

Author keywords

EEG fMRI; Mesial temporal lobe epilepsy; Network analysis; Voxel based morphometry

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN SIZE; CENTRAL SULCUS; CEREBELLUM; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EPILEPTIC DISCHARGE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HEMODYNAMICS; HIPPOCAMPUS; HUMAN; INFERIOR TEMPORAL GYRUS; INSULA; MALE; MESIAL TEMPORAL EPILEPSY; MESOLIMBIC DOPAMINERGIC SYSTEM; MIDDLE TEMPORAL GYRUS; NEOCORTEX; NEUROIMAGING; OPERCULUM (BRAIN); POSTERIOR CINGULATE; PRIORITY JOURNAL; TEMPORAL LOBE EPILEPSY; UNCUS;

ADULT; AGED; BRAIN; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; FEMALE; HEMODYNAMICS; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; SEIZURES; SIGNAL PROCESSING, COMPUTER-ASSISTED; YOUNG ADULT;

EID: 84878860828     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-013-6841-2     Document Type: Article

References (55)

1. Alarcon G, Guy CN, Binnie CD, Walker SR, Elwes RD, Polkey CE (1994) Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation. J Neurol Neurosurg Psychiatry 57:435-449 (Pubitemid 24118139)
2. Bartolomei F, Chauvel P, Wendling F (2008) Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 131:1818-1830 (Pubitemid 351957462)
3. Bartolomei F, Wendling F, Bellanger JJ, Regis J, Chauvel P (2001) Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin Neurophysiol 112:1746-1760 (Pubitemid 32763258)
4. Benuzzi F, Mirandola L, Pugnaghi M, Farinelli V, Tassinari CA, Capovilla G, Cantalupo G, Beccaria F, Nichelli P, Meletti S (2012) Increased cortical BOLD signal anticipates generalized spike and wave discharges in adolescents and adults with idiopathic generalized epilepsies. Epilepsia 53:622-630
5. Bernhardt BC, Bernasconi N, Concha L, Bernasconi A (2010) Cortical thickness analysis in temporal lobe epilepsy: reproducibility and relation to outcome. Neurology 74:1776-1784
6. Blumenfeld H, McNally KA, Vanderhill SD, Paige AL, Chung R, Davis K, Norden AD, Stokking R, Studholme C, Novotny EJ Jr, Zubal IG, Spencer SS (2004) Positive and negative network correlations in temporal lobe epilepsy. Cereb Cortex 14:892-902 (Pubitemid 38971463)
7. Bonilha L, Edwards JC, Kinsman SL, Morgan PS, Fridriksson J, Rorden C, Rumboldt Z, Roberts DR, Eckert MA, Halford JJ (2010) Extrahippocampal gray matter loss and hippocampal deafferentation in patients with temporal lobe epilepsy. Epilepsia 51:519-528
8. Bonilha L, Rorden C, Appenzeller S, Coan AC, Cendes F, Li LM (2006) Gray matter atrophy associated with duration of temporal lobe epilepsy. Neuroimage 32:1070-1079 (Pubitemid 44308283)
9. Carney PW, Masterton RA, Flanagan D, Berkovic SF, Jackson GD (2012) The frontal lobe in absence epilepsy: EEG-fMRI findings. Neurology 78:1157-1165
10. Catani M, Jones DK, Donato R, Ffytche DH (2003) Occipito-temporal connections in the human brain. Brain 126:2093-2107 (Pubitemid 37059449)
11. Chupin M, Hammers A, Liu RS, Colliot O, Burdett J, Bardinet E, Duncan JS, Garnero L, Lemieux L (2009) Automatic segmentation of the hippocampus and the amygdala driven by hybrid constraints: method and validation. Neuroimage 46:749-761
12. Coan AC, Appenzeller S, Bonilha L, Li LM, Cendes F (2009) Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy. Neurology 73:834-842
13. Cole DM, Smith SM, Beckmann CF (2010) Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front Syst Neurosci 4:8
14. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848-13853 (Pubitemid 44413996)
15. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9-21 (Pubitemid 38224183)
16. Duzel E, Schiltz K, Solbach T, Peschel T, Baldeweg T, Kaufmann J, Szentkuti A, Heinze HJ (2006) Hippocampal atrophy in temporal lobe epilepsy is correlated with limbic systems atrophy. J Neurol 253:294-300
17. Engel J Jr, Brown WJ, Kuhl DE, Phelps ME, Mazziotta JC, Crandall PH (1982) Pathological findings underlying focal temporal lobe hypometabolism in partial epilepsy. Ann Neurol 12:518-528 (Pubitemid 13250406)
18. Fahoum F, Lopes R, Pittau F, Dubeau F, Gotman J (2012) Widespread epileptic networks in focal epilepsies-EEG-fMRI study. Epilepsia 53(9):1618-1627
19. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636-647
20. Friston KJ, Stephan KE, Lund TE, Morcom A, Kiebel S (2005) Mixed-effects and fMRI studies. Neuroimage 24:244-252 (Pubitemid 39611045)
21. Gloor P, Olivier A, Quesney LF, Andermann F, Horowitz S (1982) The role of the limbic system in experiential phenomena of temporal lobe epilepsy. Ann Neurol 12:129-144 (Pubitemid 12097690)
22. Glover GH (1999) Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage 9:416-429 (Pubitemid 29369861)
23. Gotman J (2008) Epileptic networks studied with EEG-fMRI. Epilepsia 49(Suppl 3):42-51
24. Guye M, Regis J, Tamura M, Wendling F, McGonigal A, Chauvel P, Bartolomei F (2006) The role of corticothalamic coupling in human temporal lobe epilepsy. Brain 129:1917-1928 (Pubitemid 43999422)
25. Hauf M, Jann K, Schindler K, Scheidegger O, Meyer K, Rummel C, Mariani L, Koenig T, Wiest R (2012) Localizing seizure-onset zones in presurgical evaluation of drug-resistant epilepsy by electroencephalography/fMRI: effectiveness of alternative thresholding strategies. AJNR Am J Neuroradiol 33:1818-1824
26. Hesse C, James C (2005) Tracking epileptiform activity in the multichannel ictal EEG using spatially constrained independent component analysis. Conf Proc IEEE Eng Med Biol Soc 2:2067-2070 (Pubitemid 46229315)
27. Jackson GD, Badawy RA (2011) Selecting patients for epilepsy surgery: identifying a structural lesion. Epilepsy Behav 20:182-189
28. Jann K, Kottlow M, Dierks T, Boesch C, Koenig T (2010) Topographic electrophysiological signatures of FMRI resting state networks. PLoS ONE 5:e12945
29. Jann K, Wiest R, Hauf M, Meyer K, Boesch C, Mathis J, Schroth G, Dierks T, Koenig T (2008) BOLD correlates of continuously fluctuating epileptic activity isolated by independent component analysis. Neuroimage 42:635-648
30. Keller SS, Mackay CE, Barrick TR, Wieshmann UC, Howard MA, Roberts N (2002) Voxel-based morphometric comparison of hippocampal and extrahippocampal abnormalities in patients with left and right hippocampal atrophy. Neuroimage 16:23-31 (Pubitemid 34852469)
31. Khan AR, Wang L, Beg MF (2008) FreeSurfer-initiated fully-automated subcortical brain segmentation in MRI using large deformation diffeomorphic metric mapping. Neuroimage 41:735-746
32. Kobayashi E, Grova C, Tyvaert L, Dubeau F, Gotman J (2009) Structures involved at the time of temporal lobe spikes revealed by interindividual group analysis of EEG/fMRI data. Epilepsia 50:2549-2556
33. Krendl R, Lurger S, Baumgartner C (2008) Absolute spike frequency predicts surgical outcome in TLE with unilateral hippocampal atrophy. Neurology 71:413-418
34. Larsen S, Kikinis R, Talos IF, Weinstein D, Wells W, Golby A (2007) Quantitative comparison of functional MRI and direct electrocortical stimulation for functional mapping. Int J Med Robot 3:262-270 (Pubitemid 350033316)
35. Laufs H, Hamandi K, Salek-Haddadi A, Kleinschmidt AK, Duncan JS, Lemieux L (2007) Temporal lobe interictal epileptic discharges affect cerebral activity in "default mode" brain regions. Hum Brain Mapp 28:1023-1032 (Pubitemid 47549706)
36. Li B, Wang X, Yao S, Hu D, Friston K (2012) Task-dependent modulation of effective connectivity within the default mode network. Front Psychol 3:206
37. Luders E, Gaser C, Jancke L, Schlaug G (2004) A voxel-based approach to gray matter asymmetries. Neuroimage 22:656-664 (Pubitemid 38759428)
38. Luo C, Qiu C, Guo Z, Fang J, Li Q, Lei X, Xia Y, Lai Y, Gong Q, Zhou D, Yao D (2011) Disrupted functional brain connectivity in partial epilepsy: a resting-state fMRI study. PLoS ONE 7:e28196
39. Maillard L, Vignal JP, Gavaret M, Guye M, Biraben A, McGonigal A, Chauvel P, Bartolomei F (2004) Semiologic and electrophysiologic correlations in temporal lobe seizure subtypes. Epilepsia 45:1590-1599 (Pubitemid 39648284)
40. Meisenzahl EM, Koutsouleris N, Gaser C, Bottlender R, Schmitt GJ, McGuire P, Decker P, Burgermeister B, Born C, Reiser M, Moller HJ (2008) Structural brain alterations in subjects at high-risk of psychosis: a voxel-based morphometric study. Schizophr Res 102:150-162
41. Moorhead TW, Job DE, Spencer MD, Whalley HC, Johnstone EC, Lawrie SM (2005) Empirical comparison of maximal voxel and non-isotropic adjusted cluster extent results in a voxel-based morphometry study of comorbid learning disability with schizophrenia. Neuroimage 28:544-552 (Pubitemid 41540365)
42. Mueller SG, Laxer KD, Barakos J, Cheong I, Garcia P, Weiner MW (2009) Widespread neocortical abnormalities in temporal lobe epilepsy with and without mesial sclerosis. Neuroimage 46:353-359
43. Oakes TR, Fox AS, Johnstone T, Chung MK, Kalin N, Davidson RJ (2007) Integrating VBM into the general linear model with voxelwise anatomical covariates. Neuroimage 34:500-508 (Pubitemid 44827773)
44. Pail M, Brazdil M, Marecek R, Mikl M (2010) An optimized voxel-based morphometric study of gray matter changes in patients with left-sided and right-sided mesial temporal lobe epilepsy and hippocampal sclerosis (MTLE/HS). Epilepsia 51:511-518
45. Riederer F, Lanzenberger R, Kaya M, Prayer D, Serles W, Baumgartner C (2008) Network atrophy in temporal lobe epilepsy: a voxel-based morphometry study. Neurology 71:419-425
46. Santana MT, Jackowski AP, da Silva HH, Caboclo LO, Centeno RS, Bressan RA, Carrete H Jr, Yacubian EM (2010) Auras and clinical features in temporal lobe epilepsy: a new approach on the basis of voxel-based morphometry. Epilepsy Res 89:327-338
47. Spencer SS (2002) Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 43:219-227 (Pubitemid 34260378)
48. Sutula TP, Hagen J, Pitkanen A (2003) Do epileptic seizures damage the brain? Curr Opin Neurol 16:189-195 (Pubitemid 36521206)
49. Tao JX, Chen XJ, Baldwin M, Yung I, Rose S, Frim D, Hawes-Ebersole S, Ebersole JS (2011) Interictal regional delta slowing is an EEG marker of epileptic network in temporal lobe epilepsy. Epilepsia 52:467-476
50. Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309:2226-2228 (Pubitemid 41396074)
51. Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, Buckner RL (2006) Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96:3517-3531 (Pubitemid 44837893)
52. Voets NL, Beckmann CF, Cole DM, Hong S, Bernasconi A, Bernasconi N (2012) Structural substrates for resting network disruption in temporal lobe epilepsy. Brain 135(Pt 8):2350-2357
53. Weder BJ, Schindler K, Loher TJ, Wiest R, Wissmeyer M, Ritter P, Lovblad K, Donati F, Missimer J (2006) Brain areas involved in medial temporal lobe seizures: a principal component analysis of ictal SPECT data. Hum Brain Mapp 27:520-534 (Pubitemid 43902417)
54. Zhang Z, Lu G, Zhong Y, Tan Q, Liao W, Chen Z, Shi J, Liu Y (2009) Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI. J Neurol 256:1705-1713
55. Zheng J, Qin B, Dang C, Ye W, Chen Z, Yu L (2012) Alertness network in patients with temporal lobe epilepsy: a fMRI study. Epilepsy Res 100:67-73