DOI QR코드

DOI QR Code

Gray, White Matter Concentration Changes and Their Correlation with Heterotopic Neurons in Temporal Lobe Epilepsy

  • Tae, Woo-Suk (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Joo, Eun-Yun (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Kim, Sung-Tae (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Hong, Seung-Bong (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine)
  • Received : 2009.01.27
  • Accepted : 2009.08.27
  • Published : 2010.02.01

Abstract

Objective: To identify changes in gray and white matter concentrations (GMC, WMC), and their relation to heterotopic neuron numbers in mesial temporal lobe epilepsy (mTLE). Materials and Methods: The gray matter or white matter concentrations of 16 left and 15 right mTLE patients who achieved an excellent surgical outcome were compared with those of 24 healthy volunteers for the left group and with 23 healthy volunteers for the right group, by optimized voxel-based morphometry using unmodulated and modulated images. A histologic count of heterotopic neurons was obtained in the white matter of the anterior temporal lobe originating from the patients' surgical specimens. In addition, the number of heterotopic neurons were tested to determine if there was a correlation with the GMC or WMC. Results: The GMCs of the left and right mTLE groups were reduced in the ipsilateral hippocampi, bilateral thalami, precentral gyri, and in the cerebellum. The WMCs were reduced in the ipsilateral white matter of the anterior temporal lobe, bilateral parahippocampal gyri, and internal capsules, but increased in the pons and bilateral precentral gyri. The heterotopic neuron counts in the left mTLE group showed a positive correlation (r = 0.819, p < 0.0001) with GMCs and a negative correlation (r = - 0.839, p < 0.0001) with WMCs in the white matter of the anterior temporal lobe. Conclusion: The present study shows the abnormalities of the cortico-thalamo- hippocampal network including a gray matter volume reduction in the anterior frontal lobes and an abnormality of brain tissue concentration in the pontine area. Furthermore, heterotopic neuron numbers were significantly correlated with GMC or WMC in the left white matter of anterior temporal lobe.

Keywords

Acknowledgement

Supported by : Samsung Biomedical Research Institute, Korea Research Foundation

References

  1. Bernasconi N, Duchesne S, Janke A, Lerch J, Collins DL, Bernasconi A. Whole-brain voxel-based statistical analysis of gray matter and white matter in temporal lobe epilepsy. Neuroimage 2004;23:717-723 https://doi.org/10.1016/j.neuroimage.2004.06.015
  2. Bonilha L, Rorden C, Castellano G, Cendes F, Li LM. Voxel-based morphometry of the thalamus in patients with refractory medial temporal lobe epilepsy. Neuroimage 2005;25:1016-1021 https://doi.org/10.1016/j.neuroimage.2004.11.050
  3. Bonilha L, Rorden C, Castellano G, Pereira F, Rio PA, Cendes F, et al. Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Arch Neurol 2004;61:1379-1384 https://doi.org/10.1001/archneur.61.9.1379
  4. Wehner T, Luders H. Role of neuroimaging in the presurgical evaluation of epilepsy. J Clin Neurol 2008;4:1-16 https://doi.org/10.3988/jcn.2008.4.1.1
  5. McMillan AB, Hermann BP, Johnson SC, Hansen RR, Seidenberg M, Meyerand ME. Voxel-based morphometry of unilateral temporal lobe epilepsy reveals abnormalities in cerebral white matter. Neuroimage 2004;23:167-174 https://doi.org/10.1016/j.neuroimage.2004.05.002
  6. Duzel E, Schiltz K, Solbach T, Peschel T, Baldeweg T, Kaufmann J, et al. Hippocampal atrophy in temporal lobe epilepsy is correlated with limbic systems atrophy. J Neurol 2006;253:294-300 https://doi.org/10.1007/s00415-005-0981-y
  7. Choi D, Na DG, Byun HS, Suh YL, Kim SE, Ro DW, et al. White-matter change in mesial temporal sclerosis: correlation of MRI with PET, pathology, and clinical features. Epilepsia 1999;40:1634-1641 https://doi.org/10.1111/j.1528-1157.1999.tb02050.x
  8. Hammers A, Koepp MJ, Hurlemann R, Thom M, Richardson MP, Brooks DJ, et al. Abnormalities of grey and white matter [11C] flumazenil binding in temporal lobe epilepsy with normal MRI. Brain 2002;125:2257-2271 https://doi.org/10.1093/brain/awf233
  9. Tae WS, Joo EY, Kim JH, Han SJ, Suh YL, Kim BT, et al. Cerebral perfusion changes in mesial temporal lobe epilepsy: SPM analysis of ictal and interictal SPECT. Neuroimage 2005;24:101-110 https://doi.org/10.1016/j.neuroimage.2004.08.005
  10. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001;14:21-36 https://doi.org/10.1006/nimg.2001.0786
  11. Duvernoy HM. The human brain: surface, three-dimensional sectional anatomy, and MRI, and blood supply. New York: Springer-Verlag, 1999
  12. Keller SS, Mackay CE, Barrick TR, Wieshmann UC, Howard MA, Roberts N. Voxel-based morphometric comparison of hippocampal and extrahippocampal abnormalities in patients with left and right hippocampal atrophy. Neuroimage 2002;16:23-31 https://doi.org/10.1006/nimg.2001.1072
  13. Keller SS, Wieshmann UC, Mackay CE, Denby CE, Webb J, Roberts N. Voxel based morphometry of grey matter abnormalities in patients with medically intractable temporal lobe epilepsy: effects of side of seizure onset and epilepsy duration. J Neurol Neurosurg Psychiatry 2002;73:648-655 https://doi.org/10.1136/jnnp.73.6.648
  14. Mueller SG, Laxer KD, Cashdollar N, Buckley S, Paul C, Weiner MW. Voxel-based optimized morphometry (VBM) of gray and white matter in temporal lobe epilepsy (TLE) with and without mesial temporal sclerosis. Epilepsia 2006;47:900-907 https://doi.org/10.1111/j.1528-1167.2006.00512.x
  15. Keller SS, Cresswell P, Denby C, Wieshmann U, Eldridge P, Baker G, et al. Persistent seizures following left temporal lobe surgery are associated with posterior and bilateral structural and functional brain abnormalities. Epilepsy Res 2007;74:131-139 https://doi.org/10.1016/j.eplepsyres.2007.02.005
  16. Dlugos DJ, Jaggi J, O'Connor WM, Ding XS, Reivich M, O'Connor MJ, et al. Hippocampal cell density and subcortical metabolism in temporal lobe epilepsy. Epilepsia 1999;40:408-413 https://doi.org/10.1111/j.1528-1157.1999.tb00734.x
  17. Jutila L, Ylinen A, Partanen K, Alafuzoff I, Mervaala E, Partanen J, et al. MR volumetry of the entorhinal, perirhinal, and temporopolar cortices in drug-refractory temporal lobe epilepsy. AJNR Am J Neuroradiol 2001;22:1490-1501
  18. Lee HW, Hong SB, Tae WS. Opposite ictal perfusion patterns of subtracted SPECT. Hyperperfusion and hypoperfusion. Brain 2000;123:2150-2159 https://doi.org/10.1093/brain/123.10.2150
  19. Rabinowicz AL, Salas E, Beserra F, Leiguarda RC, Vazquez SE. Changes in regional cerebral blood flow beyond the temporal lobe in unilateral temporal lobe epilepsy. Epilepsia 1997;38:1011-1014 https://doi.org/10.1111/j.1528-1157.1997.tb01484.x
  20. Prince DA, Wilder BJ. Control mechanisms in cortical epileptogenic foci. "Surround" inhibition. Arch Neurol 1967;16:194-202 https://doi.org/10.1001/archneur.1967.00470200082007
  21. Lieb JP, Dasheiff RM, Engel J Jr. Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 1991;32:822-837 https://doi.org/10.1111/j.1528-1157.1991.tb05539.x
  22. Arfanakis K, Hermann BP, Rogers BP, Carew JD, Seidenberg M, Meyerand ME. Diffusion tensor MRI in temporal lobe epilepsy. Magn Reson Imaging 2002;20:511-519 https://doi.org/10.1016/S0730-725X(02)00509-X
  23. Jack CR Jr, Twomey CK, Zinsmeister AR, Sharbrough FW, Petersen RC, Cascino GD. Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 1998;172:549-554
  24. Jack CR Jr. MRI-based hippocampal volume measurements in epilepsy. Epilepsia 1994;35:S21-S29
  25. Kim JH, Murdoch GH, Hufnagel TJ, Shen MY, Harrington WN, Spencer DD. White matter changes in intractable temporal lobe epilepsy [abstract]. Epilepsia 1990;31:630
  26. Chung MH, Horoupian DS. Corpora amylacea: a marker for mesial temporal sclerosis. J Neuropathol Exp Neurol 1996;55:403-408 https://doi.org/10.1097/00005072-199604000-00002
  27. Dreifuss S, Vingerhoets FJ, Lazeyras F, Andino SG, Spinelli L, Delavelle J, et al. Volumetric measurements of subcortical nuclei in patients with temporal lobe epilepsy. Neurology 2001;57:1636-1641 https://doi.org/10.1212/WNL.57.9.1636
  28. Lee KH, Meador KJ, Park YD, King DW, Murro AM, Pillai JJ, et al. Pathophysiology of altered consciousness during seizures: subtraction SPECT study. Neurology 2002;59:841-846 https://doi.org/10.1212/WNL.59.6.841
  29. Ashburner J, Friston KJ. Nonlinear spatial normalization using basis functions. Hum Brain Mapp 1999;7:254-266 https://doi.org/10.1002/(SICI)1097-0193(1999)7:4<254::AID-HBM4>3.0.CO;2-G
  30. Keller SS, Wilke M, Wieshmann UC, Sluming VA, Roberts N. Comparison of standard and optimized voxel-based morphometry for analysis of brain changes associated with temporal lobe epilepsy. Neuroimage 2004;23:860-868 https://doi.org/10.1016/j.neuroimage.2004.07.030

Cited by

  1. Thalamic medial dorsal nucleus atrophy in medial temporal lobe epilepsy: A VBM meta-analysis vol.2, pp.None, 2010, https://doi.org/10.1016/j.nicl.2012.11.004
  2. Meta-analysis of voxel-based morphometry studies of gray matter abnormalities in patients with mesial temporal lobe epilepsy and unilateral hippocampal sclerosis vol.12, pp.5, 2010, https://doi.org/10.1007/s11682-017-9797-5