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Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI

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Abstract

Viewed as a neural network disorder, mesial temporal lobe epilepsy (mTLE) may cause widespread deficits in human brain functions. Impairments in cognitive functions such as memory and language have been well addressed, but perceptual deficits have only been considered in terms of behavioral data. Little imaging research on perceptual deficits in mTLE has been reported. The present study is expected to reveal impairments in the perceptual networks in patients with mTLE using fMRI. The fMRI-based independent component analysis (ICA) was applied to 33 patients with mTLE and 33 matched healthy controls. In light of the resting-state networks (RSNs) corresponding to the basal functions of visual, auditory, and sensorimotor systems, the ICA data of functional connectivity within these RSNs were compared between the patients and controls. Compared with the controls, the mTLE patients presented decreased functional connectivity within the regions of the auditory and sensorimotor networks, as well increased functional connectivity in the primary visual cortex and decreased functional connectivity in the bilateral MT+ areas of the visual network. Our neuroimaging results are in agreement with the previous findings that specific perceptual functions are impaired in mTLE. Furthermore, our findings in the visual network support the belief that the primary visual function is not impaired and that there may be deficits in the high-order visual function in mTLE. Our fMRI study may contribute to the understanding of neuropathophysiological mechanisms underlying perceptual impairments in mTLE.

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References

  1. Adcock JE, Wise RG, Oxbury JM, Oxbury SM, Matthews PM (2003) Quantitative fMRI assessment of the differences in lateralization of language-related brain activation in patients with temporal lobe epilepsy. Neuroimage 18:423–438. doi:10.1016/S1053-8119(02)00013-7

    Article  PubMed  CAS  Google Scholar 

  2. Bagshaw AP, Torab L, Kobayashi E, Hawco C, Dubeau F, Pike GB, Gotman J (2006) EEG-fMRI using z-shimming in patients with temporal lobe epilepsy. J Magn Reson Imaging 24:1025–1032. doi:10.1002/jmri.20744

    Article  PubMed  Google Scholar 

  3. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001–1013. doi:10.1098/rstb.2005.1634

    Article  PubMed  Google Scholar 

  4. Beckung E, Uvebrant P (1993) Motor and sensory impairments in children with intractable epilepsy. Epilepsia 34:924–929. doi:10.1111/j.1528-1157.1993.tb02113.x

    Article  PubMed  CAS  Google Scholar 

  5. Bettus G, Guedj E, Joyeux F, Confort-Gouny S, Soulier E, Laguitton V, Cozzone PJ, Chauvel P, Ranjeva JP, Bartolomei F, Guye M (2008) Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms. Hum Brain Mapp 30:1580–1591. doi:10.1002/hbm.20625

    Google Scholar 

  6. Billingsley RL, McAndrews MP, Crawley AP, Mikulis DJ (2001) Functional MRI of phonological and semantic processing in temporal lobe epilepsy. Brain 124:1218–1227. doi:10.1093/brain/124.6.1218

    Article  PubMed  CAS  Google Scholar 

  7. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541. doi:10.1002/mrm.1910340409

    Article  PubMed  CAS  Google Scholar 

  8. Biswal BB, Van Kylen J, Hyde JS (1997) Simultaneous assessment of flow and BOLD signals in resting-state functional connectivity maps. NMR Biomed 10:165–170. doi:10.1002/(SICI)1099-1492(199706/08)10:4/5<165::AID-NBM454>3.0.CO;2-7

    Article  PubMed  CAS  Google Scholar 

  9. 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. doi:10.1093/cercor/bhh048

    Article  PubMed  Google Scholar 

  10. Buckner RL, Vincent JL (2007) Unrest at rest: default activity and spontaneous network correlations. Neuroimage 37:1091–1096. doi:10.1016/j.neuroimage.2007.01.010 discussion 1097–1099

    Article  PubMed  Google Scholar 

  11. Calhoun VD, Kiehl KA, Pearlson GD (2008) Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Hum Brain Mapp 29:828–838. doi:10.1002/hbm.20581

    Article  PubMed  Google Scholar 

  12. Cascino GD (2006) A cerebral network reflecting reorganization in medial temporal lobe epilepsy. Epilepsy Curr 6:46–48. doi:10.1111/j.1535-7511.2006.00098.x

    Article  PubMed  Google Scholar 

  13. 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. doi:10.1073/pnas.0601417103

    Article  PubMed  CAS  Google Scholar 

  14. De Luca M, Beckmann CF, De Stefano N, Matthews PM, Smith SM (2006) fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29:1359–1367. doi:10.1016/j.neuroimage.2005.08.035

    Article  PubMed  Google Scholar 

  15. Del Vecchio N, Liporace J, Nei M, Sperling M, Tracy J (2004) A dissociation between implicit and explicit verbal memory in left temporal lobe epilepsy. Epilepsia 45:1124–1133. doi:10.1111/j.0013-9580.2004.28903.x

    Article  PubMed  Google Scholar 

  16. Ehrle N, Samson S, Baulac M (2001) Processing of rapid auditory information in epileptic patients with left temporal lobe damage. Neuropsychologia 39:525–531. doi:10.1016/S0028-3932(00)00121-4

    Article  PubMed  CAS  Google Scholar 

  17. Englot DJ, Mishra AM, Mansuripur PK, Herman P, Hyder F, Blumenfeld H (2008) Remote effects of focal hippocampal seizures on the rat neocortex. J Neurosci 28:9066–9081. doi:10.1523/JNEUROSCI.2014-08.2008

    Article  PubMed  CAS  Google Scholar 

  18. Erickson JC, Clapp LE, Ford G, Jabbari B (2006) Somatosensory auras in refractory temporal lobe epilepsy. Epilepsia 47:202–206. doi:10.1111/j.1528-1167.2006.00388.x

    Article  PubMed  Google Scholar 

  19. Fox MD, Corbetta M, Snyder AZ, Vincent JL, Raichle ME (2006) Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc Natl Acad Sci USA 103:10046–10051. doi:10.1073/pnas.0604187103

    Article  PubMed  CAS  Google Scholar 

  20. Garrity AG, Pearlson GD, McKiernan K, Lloyd D, Kiehl KA, Calhoun VD (2007) Aberrant “default mode” functional connectivity in schizophrenia. Am J Psychiatry 164:450–457. doi:10.1176/appi.ajp.164.3.450

    Article  PubMed  Google Scholar 

  21. Gotman J, Kobayashi E, Bagshaw AP, Benar CG, Dubeau F (2006) Combining EEG and fMRI: a multimodal tool for epilepsy research. J Magn Reson Imaging 23:906–920. doi:10.1002/jmri.20577

    Article  PubMed  Google Scholar 

  22. Grant AC (2005) Interictal perceptual function in epilepsy. Epilepsy Behav 6:511–519. doi:10.1016/j.yebeh.2005.03.016

    Article  PubMed  Google Scholar 

  23. Grant AC, Donnelly KM, Chubb C, Barr WB, Kuzniecky R, Devinsky O (2008) Temporal lobe epilepsy does not impair visual perception. Epilepsia 49:710–713. doi:10.1111/j.1528-1167.2007.01483.x

    Article  PubMed  Google Scholar 

  24. Grant AC, Fujikawa S, Zeng F (2008) Central auditory function in temporal lobe epilepsy. Epilepsia 42(Suppl 7):249

    Google Scholar 

  25. Grant AC, Henry TR, Fernandez R, Hill MA, Sathian K (2005) Somatosensory processing is impaired in temporal lobe epilepsy. Epilepsia 46:534–539. doi:10.1111/j.0013-9580.2005.54604.x

    Article  PubMed  Google Scholar 

  26. Greicius MD, Kiviniemi V, Tervonen O, Vainionpaa V, Alahuhta S, Reiss AL, Menon V (2008) Persistent default-mode network connectivity during light sedation. Hum Brain Mapp 29:839–847. doi:10.1002/hbm.20537

    Article  PubMed  Google Scholar 

  27. 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 USA 100:253–258. doi:10.1073/pnas.0135058100

    Article  PubMed  CAS  Google Scholar 

  28. Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101:4637–4642. doi:10.1073/pnas.0308627101

    Article  PubMed  CAS  Google Scholar 

  29. Hamandi K, Powell HW, Laufs H, Symms MR, Barker GJ, Parker GJ, Lemieux L, Duncan JS (2008) Combined EEG-fMRI and tractography to visualise propagation of epileptic activity. J Neurol Neurosurg Psychiatry 79:594–597. doi:10.1136/jnnp.2007.125401

    Article  PubMed  CAS  Google Scholar 

  30. Hamberger MJ, McClelland S III, McKhann GM II, Williams AC, Goodman RR (2007) Distribution of auditory and visual naming sites in nonlesional temporal lobe epilepsy patients and patients with space-occupying temporal lobe lesions. Epilepsia 48:531–538. doi:10.1111/j.1528-1167.2006.00955.x

    Article  PubMed  Google Scholar 

  31. Hilton EJ, Cubbidge RP, Hosking SL, Betts T, Comaish IF (2002) Patients treated with vigabatrin exhibit central visual function loss. Epilepsia 43:1351–1359. doi:10.1046/j.1528-1157.2002.00502.x

    Article  PubMed  Google Scholar 

  32. Jafri MJ, Pearlson GD, Stevens M, Calhoun VD (2008) A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 39:1666–1681. doi:10.1016/j.neuroimage.2007.11.001

    Article  PubMed  Google Scholar 

  33. Kobayashi E, Bagshaw AP, Benar CG, Aghakhani Y, Andermann F, Dubeau F, Gotman J (2006) Temporal and extratemporal BOLD responses to temporal lobe interictal spikes. Epilepsia 47:343–354. doi:10.1111/j.1528-1167.2006.00427.x

    Article  PubMed  Google Scholar 

  34. 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. doi:10.1002/hbm.20323

    Article  PubMed  Google Scholar 

  35. Li YO, Adali T, Calhoun VD (2007) Estimating the number of independent components for functional magnetic resonance imaging data. Hum Brain Mapp 28:1251–1266. doi:10.1002/hbm.20359

    Article  PubMed  Google Scholar 

  36. Mantini D, Corbetta M, Perrucci MG, Romani GL, Del Gratta C (2009) Large-scale brain networks account for sustained and transient activity during target detection. Neuroimage 44:265–274. doi:10.1016/j.neuroimage.2008.08.019

    Article  PubMed  Google Scholar 

  37. Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M (2007) Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci USA 104:13170–13175. doi:10.1073/pnas.0700668104

    Article  PubMed  CAS  Google Scholar 

  38. Mazzucchi A, Visintini D, Magnani G, Cattelani R, Parma M (1985) Hemispheric prevalence changes in partial epileptic patients on perceptual and attentional tasks. Epilepsia 26:379–390. doi:10.1111/j.1528-1157.1985.tb05668.x

    Article  PubMed  CAS  Google Scholar 

  39. Nelissen N, Van Paesschen W, Baete K, Van Laere K, Palmini A, Van Billoen H, Dupont P (2006) Correlations of interictal FDG-PET metabolism and ictal SPECT perfusion changes in human temporal lobe epilepsy with hippocampal sclerosis. Neuroimage 32:684–695. doi:10.1016/j.neuroimage.2006.04.185

    Article  PubMed  CAS  Google Scholar 

  40. Poline JB, Worsley KJ, Evans AC, Friston KJ (1997) Combining spatial extent and peak intensity to test for activations in functional imaging. Neuroimage 5:83–96. doi:10.1006/nimg.1996.0248

    Article  PubMed  CAS  Google Scholar 

  41. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98:676–682. doi:10.1073/pnas.98.2.676

    Article  PubMed  CAS  Google Scholar 

  42. Silva AV, Sanabria ER, Cavalheiro EA, Spreafico R (2002) Alterations of the neocortical GABAergic system in the pilocarpine model of temporal lobe epilepsy: neuronal damage and immunocytochemical changes in chronic epileptic rats. Brain Res Bull 58:417–421. doi:10.1016/S0361-9230(02)00811-0

    Article  PubMed  CAS  Google Scholar 

  43. Spencer SS (2002) Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 43:219–227. doi:10.1046/j.1528-1157.2002.26901.x

    Article  PubMed  Google Scholar 

  44. Tae WS, Joo EY, Kim JH, Han SJ, Suh YL, Kim BT, Hong SC, Hong SB (2005) Cerebral perfusion changes in mesial temporal lobe epilepsy: SPM analysis of ictal and interictal SPECT. Neuroimage 24:101–110. doi:10.1016/j.neuroimage.2004.08.005

    Article  PubMed  Google Scholar 

  45. Trinka E, Unterrainer J, Luef G, Ladurner G (2001) Multimodal P3 under different attentional states in mesial temporal lobe epilepsy. Eur J Neurol 8:261–266. doi:10.1046/j.1468-1331.2001.00214.x

    Article  PubMed  CAS  Google Scholar 

  46. van Rooyen F, Young NA, Larson SE, Teskey GC (2006) Hippocampal kindling leads to motor map expansion. Epilepsia 47:1383–1391. doi:10.1111/j.1528-1167.2006.00604.x

    Article  PubMed  Google Scholar 

  47. Vannest J, Szaflarski JP, Privitera MD, Schefft BK, Holland SK (2008) Medial temporal fMRI activation reflects memory lateralization and memory performance in patients with epilepsy. Epilepsy Behav 12:410–418. doi:10.1016/j.yebeh.2007.11.012

    Article  PubMed  Google Scholar 

  48. Vannucci M, Dietl T, Pezer N, Viggiano MP, Helmstaedter C, Schaller C, Elger CE, Grunwald T (2003) Hippocampal function and visual object processing in temporal lobe epilepsy. Neuroreport 14:1489–1492. doi:10.1097/00001756-200308060-00017

    Article  PubMed  CAS  Google Scholar 

  49. Waites AB, Briellmann RS, Saling MM, Abbott DF, Jackson GD (2006) Functional connectivity networks are disrupted in left temporal lobe epilepsy. Ann Neurol 59:335–343. doi:10.1002/ana.20733

    Article  PubMed  Google Scholar 

  50. Wu JW, Song ZQ, Chen JQ, Tan QF, Li SJ, Lu GM, Zhang ZJ, Liu YX (1998) Volumetric measurement of hippocampal formation using MRI in patients with epilepsy (in Chinese). Chin J Radiol 32:224–227

    Google Scholar 

  51. Wu JW, Song ZQ, Chen JQ, Tan QF, Li SJ, Lu GM, Zhang ZJ, Liu YX (1998) Volumetric measurement of hippocampal formation using MRI in the normal Chinese adults (in Chinese). Chin J Radiol 32:220–223

    Google Scholar 

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Acknowledgements

We thank Dr. Mantini for providing us the RSN images that were used as the templates in the present study. This work was supported by grants from the Natural Scientific Foundation of China (30470510 to Guangming Lu, 30800264 to Zhiqiang Zhang, 60628101 to Yijun Liu) and the local key projects of medical research (grant nos. 07z030 to Guangming Lu, Q2008063 to Zhiqiang Zhang). We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

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None of the authors has any conflict of interest to disclose.

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Correspondence to Guangming Lu.

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Zhang, Z., Lu, G., Zhong, Y. et al. Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI. J Neurol 256, 1705–1713 (2009). https://doi.org/10.1007/s00415-009-5187-2

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