Abstract
Mesial temporal lobe epilepsy (mTLE) with mesial temporal sclerosis (MTS) is a recognized epilepsy syndrome which is successfully treated with mesial temporal lobe resection. However, recent studies suggest that mTLE is more than a “focal” disease process. The objective of our study was to determine the presence and extent of functional abnormalities outside of a defined structural abnormality in epilepsy patients with mTLE. We used a prospective age-matched controlled design to study eight consecutive patients with MTS who were undergoing epilepsy surgery evaluation. Magnetoencephalography was used to localize the sources of electromagnetic abnormality. Proton magnetic resonance spectroscopy (1H-MRS) measured integrated peak areas for N-acetyl compounds (NAA) and choline-containing compounds (Cho) to determine regions of metabolic abnormality. All eight subjects had predominant electromagnetic abnormality in the temporal lobe ipsilateral to the MTS. All eight subjects had lower NAA/Cho ratios in the region of electromagnetic abnormality when compared to the homologous contralateral region (P < 0.001). Four subjects had predominant MEG spiking outside the mesial temporal region. Surgery-free outcome for the group with neuroimaging abnormalities outside of the medial temporal lobe is 50%. The region of maximal electromagnetic abnormality is outside the hippocampus in some patients with mTLE. These regions also demonstrate functional abnormalities. Our findings support the concept that mTLE is a more diffuse process than the hippocampal structural abnormality, which may impact surgical outcome.
Similar content being viewed by others
References
Alarcon G, Garcia Seoane JJ, Binnie CD, Martin Miguel MC, Juler J, Polkey CE, Elwes RD, Ortiz Blasco JM (1997) Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. Brain 120 (Pt 12): 2259–2282
Arnold S, Schlaug G, Niemann H, Ebner A, Lüders H, Witte OW, Seitz RJ (1996) Topography of interictal glucose hypometabolism in unilateral mesiotemporal epilepsy. Neurology 46(5):1422–1430
Babb TL, Wilson CL, Isokawa-Akesson M (1987) Firing patterns of human limbic neurons during stereoencephalography (SEEG) and clinical temporal lobe seizures. Electroencephalogr Clin Neurophysiol 66(6):467–482
Bernasconi A, Tasch E, Cendes F, Li LM, Arnold DL (2002) Proton magnetic resonance spectroscopic imaging suggests progressive neuronal damage in human temporal lobe epilepsy. Prog Brain Res 135:297–304
Cascino G, Jack CR (1996) Neuroimaging in epilepsy : principles and practice. Butterworth-Heinemann, Boston
Cendes F, Andermann F, Preul MC, Arnold DL (1994) Lateralization of temporal lobe epilepsy based on regional metabolic abnormalities in proton magnetic resonance spectroscopic images. Ann Neurol 35(2):211–216
Cendes F, Andermann F, Dubeau F, Matthews PM, Arnold DL (1997) Normalization of neuronal metabolic dysfunction after surgery for temporal lobe epilepsy. Evidence from proton MR spectroscopic imaging. Neurology 49(6):1525–1533
Chiappa KH, Hill RA, Huang-Hellinger F, Jenkins BG (1999) Photosensitive epilepsy studied by functional magnetic resonance imaging and magnetic resonance spectroscopy. Epilepsia 40(Suppl 4):3–7
Cohen D, Cuffin BN, Yunokuchi K, Maniewski R, Purcell C, Cosgrove GR et al (1990) MEG versus EEG localization test using implanted sources in the human brain. Ann Neurol 28(6):811–817
Connelly A, Jackson GD, Duncan JS, King MD, Gadian DG (1994) Magnetic resonance spectroscopy in temporal lobe epilepsy. Neurology 44(8):1411–1417
Connelly A, Van Paesschen W, Porter DA, Johnson CL, Duncan JS, Gadian DG (1998) Proton magnetic resonance spectroscopy in MRI-negative temporal lobe epilepsy. Neurology 51(1):61–66
Constantinidis I (2000) MRS methodology. Adv Neurol 83:235–246
Engel J (2007) Epilepsy: a comprehensive textbook, 2nd edn. Lippincott Williams and Wilkins, Philadelphia
Gilliam FG, Maton BM, Martin RC, Sawrie SM, Faught RE, Hugg JW, Viikinsalo M, Kuzniecky RI (2007) Hippocampal 1H-MRSI correlates with severity of depression symptoms in temporal lobe epilepsy. Neurology 68(5):364–368
Griner PF, Mayewski RJ, Mushlin AI, Greenland P (1981) Selection and interpretation of diagnostic tests and procedures. Principles and applications. Ann Intern Med 94 (4 Pt 2):557–592
Iwasaki M, Nakasato N, Shamoto H, Nagamatsu K, Kanno A, Hatanaka K et al (2002) Surgical implications of neuromagnetic spike localization in temporal lobe epilepsy. Epilepsia 43(4):415–424
Klem GH, Luders HO, Jasper HH, Elger C (1999) The ten–twenty electrode system of the international federation. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 52:3–6
Knowlton RC, Laxer KD, Aminoff MJ, Roberts TP, Wong ST, Rowley HA (1997) Magnetoencephalography in partial epilepsy: clinical yield and localization accuracy. Ann Neurol 42(4):622–631
Ko DY, Kufta C, Scaffidi D, Sato S (1998) Source localization determined by magnetoencephalography and electroencephalography in temporal lobe epilepsy: comparison with electrocorticography: technical case report. Neurosurgery 42(2):414–421, discussion 421–412
Krauss GL, Lesser RP, Fisher RS, Arroyo S (1992) Anterior “cheek” electrodes are comparable to sphenoidal electrodes for the identification of ictal activity. Electroencephalogr Clin Neurophysiol 83(6):333–338
Leahy RM, Mosher JC, Spencer ME, Huang MX, Lewine JD (1998) A study of dipole localization accuracy for MEG and EEG using a human skull phantom. Electroencephalogr Clin Neurophysiol 107(2):159–173
Lee EM, Im KC, Kim JH, Lee JK, Hong SH, No YJ, Lee SA, Kim JS, Kang JK (2009) Relationship between hypometabolic patterns and ictal scalp EEG patterns in patients with unilateral hippocampal sclerosis: an FDG-PET study. Epilepsy Res 84(2–3):187–193
Lieb JP, Dasheiff RM, Engel J Jr (1991) Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 32(6):822–837
Mueller SG, Suhy J, Laxer KD, Flenniken DL, Axelrad J, Capizzano AA et al (2002) Reduced extrahippocampal NAA in mesial temporal lobe epilepsy. Epilepsia 43(10):1210–1216
Multani P, Myers RH, Blume HW, Schomer DL, Sotrel A (1994) Neocortical dendritic pathology in human partial epilepsy: a quantitative Golgi study. Epilepsia 35(4):728–736
Namer IJ, Bolo NR, Sellal F, Nguyen VH, Nedelec JF, Hirsch E et al (1999) Combined measurements of hippocampal N-acetyl-aspartate and T2 relaxation time in the evaluation of mesial temporal lobe epilepsy: correlation with clinical severity and memory performances. Epilepsia 40(10):1424–1432
Ochi A, Otsubo H (2008) Magnetoencephalography-guided epilepsy surgery for children with intractable focal epilepsy: sickkids experience. Int J Psychophysiol 68(2):104–110
Rosenow F, Lüders H (2001) Presurgical evaluation of epilepsy. Brain 124(Pt 9):1683–1700
Savic I, Altshuler L, Baxter L, Engel J Jr (1997) Pattern of interictal hypometabolism in PET scans with fludeoxyglucose F 18 reflects prior seizure types in patients with mesial temporal lobe seizures. Arch Neurol 54(2):129–136
Shih JJ, Weisend MP, Lewine J, Sanders J, Dermon J, Lee R (2004) Areas of interictal spiking are associated with metabolic dysfunction in MRI-negative temporal lobe epilepsy. Epilepsia Mar 45(3):223–229
Stefan H, Schuler P, Abraham-Fuchs K, Schneider S, Gebhardt M, Neubauer U et al (1994) Magnetic source localization and morphological changes in temporal lobe epilepsy: comparison of MEG/EEG, ECoG and volumetric MRI in presurgical evaluation of operated patients. Acta Neurol Scand Suppl 152:83–88
Vermathen P, Ende G, Laxer KD, Knowlton RC, Matson GB, Weiner MW (1997) Hippocampal N-acetylaspartate in neocortical epilepsy and mesial temporal lobe epilepsy. Ann Neurol 42(2):194–199
Vermathen P, Ende G, Laxer KD, Walker JA, Knowlton RC, Barbaro NM et al (2002) Temporal lobectomy for epilepsy: recovery of the contralateral hippocampus measured by (1)H MRS. Neurology 59(4):633–636
Vermathen P, Laxer KD, Schuff N, Matson GB, Weiner MW (2003) Evidence of neuronal injury outside the medial temporal lobe in temporal lobe epilepsy: N-acetylaspartate concentration reductions detected with multisection proton MR spectroscopic imaging–initial experience. Radiology 226(1):195–202
Zweig MH, Campbell G (1993) Receiver operatring characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem 39(4):561–577
Acknowledgements
This work was supported by NIH/NCRR M01 RR00997-20S3 (J.J.S.), the UNM General Clinical Research Center, and NIH/NCRR COBRE 5P20RR15636 (J.J.S., M.W., R.R.L.).We thank Jeffrey Lewine, Ph.D. and John Davis, Ph.D., for technical MEG analysis.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shih, J.J., Weisend, M.P., Sanders, J.A. et al. Magnetoencephalographic and Magnetic Resonance Spectroscopy Evidence of Regional Functional Abnormality in Mesial Temporal Lobe Epilepsy. Brain Topogr 23, 368–374 (2011). https://doi.org/10.1007/s10548-010-0156-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-010-0156-8