Lennox-Gastaut综合征中的认知网络异常相互作用:可能的癫痫脑病发生机制_Journal of Epilepsy

Authors：

 AaronEL Warren , DavidF Abbott , DavidN Vaughan , 高慧 , 慕洁

Corresponding author：

AaronEL Warren, Email: a.warren@brain.org.au

Keywords：

LG综合征; 癫痫脑病; 功能磁共振; 网络; 组独立成分分析

DOI：

10.7507/2096-0247.20170069

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在Lennox-Gastaut(LG)综合征的患者中，持续反复的癫痫活动被认为是导致认知损害的原因(癫痫脑病)。使用同步脑电图-功能磁共振(EEG-fMRI)的影像手段，发现在LG综合征中癫痫放电会涉及大量在正常情况下与认知重要过程相关的网络。因此在LG综合征中，癫痫活动与认知网络相关，患者出现广泛的认知损害。就此提出假设，LG综合征认知网络间的相互作用存在持续异常。使用无任务EEG-fMRI研究了15例LG综合征患者(28.7±10.6岁)和17名健康对照者(27.6±6.6岁)。使用组独立成分分析(Group level independent components analysis，ICA)，选定4个网络用于观察(默认模式、背侧注意、执行控制及前显著网络)。对每一研究个体都进行网络内和网络间的功能连接分析后，再对比LG综合征患者和健康对照组的网络行为。为了证明在头皮未检测到放电行为时两组之间仍存在差别(即差别是持续存在的)，用足够数据对6例患者进行了放电相关和放电非相关时段的分别分析。在LG综合征中，认知网络特点为: ① 网络内部整合性减少，包括在默认模式的网络中联系更弱；② 网络之间的分离程度减低，包括默认模式和背侧注意网络间更强烈的连接。不论是否有头皮EEG的放电，fMRI上的异常相互作用均存在，表明在没有头皮能检测到的癫痫活动时也可能有异常网络行为的存在。在LG综合征中，认知网络之间相互作用关系是持续异常的。根据临床中LG综合征典型性地出现发病后认知下降，并且在癫痫得到控制后认知可能会有一定改善，该研究结果与提出的假说一致，表明LG综合征的癫痫过程可能导致并且使异常的网络行为延续。癫痫脑病的发生也许是持续存在的认知网络之间相互作用异常所导致的。

Citation： AaronEL Warren, DavidF Abbott, DavidN Vaughan, 高慧, 慕洁. Lennox-Gastaut综合征中的认知网络异常相互作用:可能的癫痫脑病发生机制. Journal of Epilepsy, 2017, 3(5): 438-448. doi: 10.7507/2096-0247.20170069 Copy

1.	Arzimanoglou A, French J, Blume WT, et al. Lennox-Gastaut syndrome: a consensus approach on diagnosis, assessment, management, and trial methodology.Lancet Neurol, 2009, 8(2): 82-93.
2.	Blume WT.Pathogenesis of Lennox-Gastaut syndrome: considerations and hypotheses.Epileptic Disord, 2002, 3(1): 183-196.
3.	Capovilla G, Moshe SL, Wolf P, et al. Epileptic encephalopathy as models of system epilepsy.Epilepsia, 2013, 54(4): 34-37.
4.	Archer JS, Warren AEL, Jackson GD, et al. Conceptualising Lennox-Gastaut Syndrome as a secondary network epilepsy.Front Neurol, 2014, 5(3): 225.
5.	Howell KB, Harvey AS, Archer JS.Epileptic encephalopathy: use and misuse of a clinically and conceptually important concept.Epilepsia, 2016, 57(3): 343-347.
6.	Oguni H, Hayashi K, Osawa M.Long-term prognosis of Lennox-Gastaut Syndrome.Epilepsia, 1996, 37(1): 44-47.
7.	van Rijckevorsel K.Treatment of Lennox-Gastaut syndrome: over-view and recent findings.Neuropsychiatr Dis Treat, 2008, 4(2): 1001-1019.
8.	Liu SY, An N, Fang X, et al. Surgical treatment of patients with Len-nox-Gastaut syndrome phenotype.Scientific World Journal, 2012, 6(4): 1-10.
9.	Smith SM, Fox PT, Miller KL, et al. Correspondence of the brain's functional architecture during activation and rest.Proc Natl Acad Sci USA, 2009, 106(11): 13040-13045.
10.	Stam CJ.Modern network science of neurological disorders.Nat Rev Neurosci, 2014, 15(4): 683-695.
11.	Biswal B, ZerrinYetkin F, Haughton VM, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.Magn Reson Med, 1995, 34(2): 537-541.
12.	Fox MD, Snyder AZ, Vincent JL, et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks.Proc Natl Acad Sci USA, 2005, 102(8): 9673-9678.
13.	Pillay N, Archer JS, Badawy RA, et al. Networks underlying paroxysmal fast activity and slow spike and wave in Lennox-Gastaut syndrome.Neurology, 2013, 81(11): 665-673.
14.	Archer JS, Warren AEL, Stagnitti MR, et al. Lennox Gastaut syndrome and phenotype: secondary network epilepsies.Epilepsia, 2014, 55(6): 1245-1254.
15.	Power JD, Barnes KA, Snyder AZ, et al. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion.Neuro Image, 2012, 59(5): 2142-2154.
16.	Masterton RA, Abbott DF, Fleming SW, et al. Measurement and reduction of motion and ballistocardiogram artefacts from simultaneous EEG and fMRI recordings.Neuro Image, 2007, 37(6): 202-211.
17.	Bhaganagarapu K, Jackson GD, Abbott DF.An automated method for identifying artifact in independent component analysis of resting-state fMRI.Front Hum Neurosci, 2013, 7(2): 343.
18.	Calhoun V, Adali T, Pearlson G, et al. A method for making group inferences from functional MRI data using independent component analysis.Hum Brain Mapp, 2001, 14(4): 140-151.
19.	Jafri MJ, Pearlson GD, Stevens M, et al. A method for functional net-Work connectivity among spatially independent resting-state compo-nents in schizophrenia.Neuro Image, 2008, 39(2): 1666-1681.
20.	Du Y, Fan Y.Group information guided ICA for fMRI data analysis.Neuro Image, 2013, 69(1): 157-197.
21.	Shirer W, Ryali S, Rykhlevskaia E, et al. Decoding subject-driven cognitive states with whole brain connectivity patterns.Cereb Cortex, 2012, 22(3): 158-165.
22.	Allen EA, Erhardt EB, Damaraju E, et al. A baseline for the multivariate comparison of resting-state networks.Front Syst Neurosci, 2011, 5(3): 2.
23.	Damoiseaux JS, Prater KE, Miller BL, et al. Functional connectivity tracks clinical deterioration in alzheimer's disease.Neurobiol Aging, 2012, 33(7): e19-30.
24.	Park JY, Kim YH, Chang WH, et al. Significance of longitudinal changes in the default mode network for cognitive recovery after stroke.Eur J Neurosci, 2014, 40(5): 2715-2722.
25.	Pizoli CE, Shah MN, Snyder AZ, et al. Resting-state activity in development and maintenance of normal brain function.Proc Natl Acad Sci USA, 2011, 108(10): 11638-11643.
26.	Kleen J, Scott R, Lenck-Santini P, et al. Cognitive and behavioral comorbidities of epilepsy.In Noebels JL, Avoli M, Rogawski MA, et al. (Eds) Jasper's basic mechanisms of the epilepsies.4th Ed.Bethesda, MD: national Center for Biotechnology Information(US), 2012: 915-929.
27.	Kleen JK, Sesqu e A, Wu EX, et al. Early life seizures produce lasting alterations in the structure and function of the prefrontal cortex.Epilepsy Behav, 2011, 22(9): 214-219.
28.	Sederberg PB, Kahana MJ, Howard MW, et al. Theta and gamma oscillations during encoding predict subsequent recall.J Neurosci, 2003, 23(5): 10809-10814.
29.	Bettus G, Ranjeva JP, Wendling F, et al. Interictal functional connec-tivity of human epileptic networks assessed by intracerebral EEG and BOLD signal fluctuations.PLoS One, 2011, 6(4): e20071.
30.	van Houdt PJ, Ossenblok PP, Colon AJ, et al. Are epilepsy-related fMRI components dependent on the presence of interictal epileptic dis-charges in scalp EEG.Brain Topogr, 2015, 28(7): 606-618.
31.	Hawco CS, Bagshaw AP, Lu Y, et al. BOLD changes occur prior to epileptic spikes seen on scalp EEG.Neuro Image, 2007, 35(8): 1450-1458.
32.	Masterton RA, Carney PW, Jackson GD.Cortical and thalamic rest-ing-state functional connectivity is altered in childhood absence epi-lepsy.Epilepsy Res, 2012, 99(11): 327-334.
33.	Terry JR, Benjamin O, Richardson MP.Seizure generation: the role of nodes and networks.Epilepsia, 2012, 53(4): e166-169.
34.	Kaiser M, Simonotto J.Limited spreading: how hierarchical networks prevent the transition to the epileptic state.In Steyn-Ross DA, Steyn-Ross M (Eds) Modeling phase transitions in the brain.New York, NY: Springer, 2010: 99-116.
35.	Pedersen M, Omidvarnia AH, Walz JM, et al. Increased segregation of brain networks in focal epilepsy: an fMRI graph theory finding.Neureimage Clin, 2015, 8(2): 536-542.
36.	Goldsmith IL, Zupanc ML, Buchhalter JR.Long-term seizure outcome in 74 patients with Lennox-Gastaut syndrome: effects of incorporating MRI head imaging in defining the cryptogenic subgroup.Epilepsia, 2000, 41(7): 395-399.
37.	Ibrahim GM, Morgan BR, Lee W, et al. Impaired development of intrinsic connectivity networks in children with medically intractable localization-related epilepsy.Hum Brain Mapp, 2014, 35(5): 5686-5700.
38.	Vaessen M, Braakman H, Heerink J, et al. Abnormal modular organi-zation of functional networks in cognitively impaired children with frontal lobe epilepsy.Cereb Cortex, 2013, 23(12): 1997-2006.
39.	Ibrahim GM, Cassel D, Morgan BR, et al. Resilience of developing brain networks to interictal epileptiform discharges is associated with cognitive outcome.Brain, 2014, 137(10): 2690-2702.
40.	Gao W, Alcauter S, Elton A, et al. Functional network development during the first year: relative sequence and socioeconomic correlations.Cereb Cortex, 2015, 25(7): 2919-2928.

1. Arzimanoglou A, French J, Blume WT, et al. Lennox-Gastaut syndrome: a consensus approach on diagnosis, assessment, management, and trial methodology.Lancet Neurol, 2009, 8(2): 82-93.
2. Blume WT.Pathogenesis of Lennox-Gastaut syndrome: considerations and hypotheses.Epileptic Disord, 2002, 3(1): 183-196.
3. Capovilla G, Moshe SL, Wolf P, et al. Epileptic encephalopathy as models of system epilepsy.Epilepsia, 2013, 54(4): 34-37.
4. Archer JS, Warren AEL, Jackson GD, et al. Conceptualising Lennox-Gastaut Syndrome as a secondary network epilepsy.Front Neurol, 2014, 5(3): 225.
5. Howell KB, Harvey AS, Archer JS.Epileptic encephalopathy: use and misuse of a clinically and conceptually important concept.Epilepsia, 2016, 57(3): 343-347.
6. Oguni H, Hayashi K, Osawa M.Long-term prognosis of Lennox-Gastaut Syndrome.Epilepsia, 1996, 37(1): 44-47.
7. van Rijckevorsel K.Treatment of Lennox-Gastaut syndrome: over-view and recent findings.Neuropsychiatr Dis Treat, 2008, 4(2): 1001-1019.
8. Liu SY, An N, Fang X, et al. Surgical treatment of patients with Len-nox-Gastaut syndrome phenotype.Scientific World Journal, 2012, 6(4): 1-10.
9. Smith SM, Fox PT, Miller KL, et al. Correspondence of the brain's functional architecture during activation and rest.Proc Natl Acad Sci USA, 2009, 106(11): 13040-13045.
10. Stam CJ.Modern network science of neurological disorders.Nat Rev Neurosci, 2014, 15(4): 683-695.
11. Biswal B, ZerrinYetkin F, Haughton VM, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.Magn Reson Med, 1995, 34(2): 537-541.
12. Fox MD, Snyder AZ, Vincent JL, et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks.Proc Natl Acad Sci USA, 2005, 102(8): 9673-9678.
13. Pillay N, Archer JS, Badawy RA, et al. Networks underlying paroxysmal fast activity and slow spike and wave in Lennox-Gastaut syndrome.Neurology, 2013, 81(11): 665-673.
14. Archer JS, Warren AEL, Stagnitti MR, et al. Lennox Gastaut syndrome and phenotype: secondary network epilepsies.Epilepsia, 2014, 55(6): 1245-1254.
15. Power JD, Barnes KA, Snyder AZ, et al. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion.Neuro Image, 2012, 59(5): 2142-2154.
16. Masterton RA, Abbott DF, Fleming SW, et al. Measurement and reduction of motion and ballistocardiogram artefacts from simultaneous EEG and fMRI recordings.Neuro Image, 2007, 37(6): 202-211.
17. Bhaganagarapu K, Jackson GD, Abbott DF.An automated method for identifying artifact in independent component analysis of resting-state fMRI.Front Hum Neurosci, 2013, 7(2): 343.
18. Calhoun V, Adali T, Pearlson G, et al. A method for making group inferences from functional MRI data using independent component analysis.Hum Brain Mapp, 2001, 14(4): 140-151.
19. Jafri MJ, Pearlson GD, Stevens M, et al. A method for functional net-Work connectivity among spatially independent resting-state compo-nents in schizophrenia.Neuro Image, 2008, 39(2): 1666-1681.
20. Du Y, Fan Y.Group information guided ICA for fMRI data analysis.Neuro Image, 2013, 69(1): 157-197.
21. Shirer W, Ryali S, Rykhlevskaia E, et al. Decoding subject-driven cognitive states with whole brain connectivity patterns.Cereb Cortex, 2012, 22(3): 158-165.
22. Allen EA, Erhardt EB, Damaraju E, et al. A baseline for the multivariate comparison of resting-state networks.Front Syst Neurosci, 2011, 5(3): 2.
23. Damoiseaux JS, Prater KE, Miller BL, et al. Functional connectivity tracks clinical deterioration in alzheimer's disease.Neurobiol Aging, 2012, 33(7): e19-30.
24. Park JY, Kim YH, Chang WH, et al. Significance of longitudinal changes in the default mode network for cognitive recovery after stroke.Eur J Neurosci, 2014, 40(5): 2715-2722.
25. Pizoli CE, Shah MN, Snyder AZ, et al. Resting-state activity in development and maintenance of normal brain function.Proc Natl Acad Sci USA, 2011, 108(10): 11638-11643.
26. Kleen J, Scott R, Lenck-Santini P, et al. Cognitive and behavioral comorbidities of epilepsy.In Noebels JL, Avoli M, Rogawski MA, et al. (Eds) Jasper's basic mechanisms of the epilepsies.4th Ed.Bethesda, MD: national Center for Biotechnology Information(US), 2012: 915-929.
27. Kleen JK, Sesqu e A, Wu EX, et al. Early life seizures produce lasting alterations in the structure and function of the prefrontal cortex.Epilepsy Behav, 2011, 22(9): 214-219.
28. Sederberg PB, Kahana MJ, Howard MW, et al. Theta and gamma oscillations during encoding predict subsequent recall.J Neurosci, 2003, 23(5): 10809-10814.
29. Bettus G, Ranjeva JP, Wendling F, et al. Interictal functional connec-tivity of human epileptic networks assessed by intracerebral EEG and BOLD signal fluctuations.PLoS One, 2011, 6(4): e20071.
30. van Houdt PJ, Ossenblok PP, Colon AJ, et al. Are epilepsy-related fMRI components dependent on the presence of interictal epileptic dis-charges in scalp EEG.Brain Topogr, 2015, 28(7): 606-618.
31. Hawco CS, Bagshaw AP, Lu Y, et al. BOLD changes occur prior to epileptic spikes seen on scalp EEG.Neuro Image, 2007, 35(8): 1450-1458.
32. Masterton RA, Carney PW, Jackson GD.Cortical and thalamic rest-ing-state functional connectivity is altered in childhood absence epi-lepsy.Epilepsy Res, 2012, 99(11): 327-334.
33. Terry JR, Benjamin O, Richardson MP.Seizure generation: the role of nodes and networks.Epilepsia, 2012, 53(4): e166-169.
34. Kaiser M, Simonotto J.Limited spreading: how hierarchical networks prevent the transition to the epileptic state.In Steyn-Ross DA, Steyn-Ross M (Eds) Modeling phase transitions in the brain.New York, NY: Springer, 2010: 99-116.
35. Pedersen M, Omidvarnia AH, Walz JM, et al. Increased segregation of brain networks in focal epilepsy: an fMRI graph theory finding.Neureimage Clin, 2015, 8(2): 536-542.
36. Goldsmith IL, Zupanc ML, Buchhalter JR.Long-term seizure outcome in 74 patients with Lennox-Gastaut syndrome: effects of incorporating MRI head imaging in defining the cryptogenic subgroup.Epilepsia, 2000, 41(7): 395-399.
37. Ibrahim GM, Morgan BR, Lee W, et al. Impaired development of intrinsic connectivity networks in children with medically intractable localization-related epilepsy.Hum Brain Mapp, 2014, 35(5): 5686-5700.
38. Vaessen M, Braakman H, Heerink J, et al. Abnormal modular organi-zation of functional networks in cognitively impaired children with frontal lobe epilepsy.Cereb Cortex, 2013, 23(12): 1997-2006.
39. Ibrahim GM, Cassel D, Morgan BR, et al. Resilience of developing brain networks to interictal epileptiform discharges is associated with cognitive outcome.Brain, 2014, 137(10): 2690-2702.
40. Gao W, Alcauter S, Elton A, et al. Functional network development during the first year: relative sequence and socioeconomic correlations.Cereb Cortex, 2015, 25(7): 2919-2928.

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Lennox-Gastaut综合征中的认知网络异常相互作用:可能的癫痫脑病发生机制

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