Connectivity disruptions in resting-state functional brain networks in children with temporal lobe epilepsy

Epilepsy Research

Volumn 100, Issue 1-2, 2012, Pages 168-178

  Mankinen, Katariina ^a   Jalovaara, Paula ^a   Paakki, Jyri Johan ^a   Harila, Marika ^a   Rytky, Seppo ^a   Tervonen, Osmo ^a   Nikkinen, Juha ^a   Starck, Tuomo ^a   Remes, Jukka ^a   Rantala, Heikki ^a   Kiviniemi, Vesa ^a  

^a OULU UNIVERSITY HOSPITAL   (Finland)

Author keywords

Default mode network; Functional connectivity; Independent component analysis; Resting state brain networks; Temporal lobe epilepsy

Indexed keywords

ADOLESCENT; ARTICLE; BRAIN FUNCTION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE DURATION; ELECTROENCEPHALOGRAPHY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; FEMALE; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; NERVE CELL NETWORK; NEUROIMAGING; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SCHOOL CHILD; TEMPORAL LOBE EPILEPSY;

ADOLESCENT; BRAIN; CHILD; EPILEPSY, TEMPORAL LOBE; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; REST;

EID: 84861526142     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2012.02.010     Document Type: Article

References (78)

1. Abou-Elseoud A., Starck T., Remes J., Nikkinen J., Tervonen O., Kiviniemi V. The effect of model order selection in group PICA. Hum. Brain Mapp. 2010, 31:1207-1216.
2. Archer J.S., Abbott D.F., Waites A.B., Jackson G.D. fMRI "deactivation" of the posterior cingulate during generalized spike and wave. Neuroimage 2003, 20:1915-1922.
3. Ashburner J., Friston K. Voxel-based morphometry - the methods. Neuroimage 2000, 11:805-821.
4. Assaf M., Jagannathan K., Calhoun V.D., Miller L., Stevens M.C., Sahl R., O'Boyle J.G., Schultz R.T., Pearlson G.D. Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. Neuroimage 2010, 53:247-256.
5. Badwy R.A.B., Harvey A.S., Macdonell R.A.L. Cortical hyperexcitability and epileptogenesis: understanding the mechanisms of epilepsy. Part 2. J. Clin. Neurosci. 2009, 16:485-500.
6. Bai X., Guo B., Killory M., Vestal R., Berman M., Negishi N., Danielson N., Novotny E.J., Constable R.T., Blumenfeld H. Resting functional connectivity between hemispheres in childhood absence epilepsy. Neurology 2011, 76:1960-1967.
7. Beckmann C.F., Smith S.M. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans. Med. Imaging 2004, 23(2):137-152.
8. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2005, 360:1001-1013.
9. Beckung E., Uvebrant P. Motor and sensory impairments in children with intractable epilepsy. Epilepsia 1993, 34:924-929.
10. Bell E.C., Wilson M.C., Wilman A.H., Dave S., Silverstone P.H. Differential effects of chronic lithium and valproate on brain activation in healthy volunteers. Hum. Psychopharmacol. 2005, 20:415-424.
11. Bettus G., Guedj E., Joyeux F., Confort-Gouny S., Soulier E., Laguitton V., Cozzone P.J., Chauvel P., Ranjev J.P., Bartolomei F., Guye M. Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms. Hum. Brain Mapp. 2009, 30:1580-1591.
12. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
13. Buckner R.L., Carroll D.C. Self-projection and the brain. Trends Cogn. Sci. 2007, 11:49-57.
14. Buckner R.L., Vincent J.L. Unrest at rest: default activity and spontaneous network correlations. Neuroimage 2007, 37:1091-1096.
15. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
16. Calhoun V.D., Adali T., Pearlson G.D., Pekar J.J. A method for making group inferences from functional MRI data using independent component analysis. Hum. Brain Mapp. 2001, 14:140-151.
17. Cao Q., Zang Y., Sun L., Sui M., Long X., Zou Q., Wang Y. Abnormal neural activity in children with attention deficit hyperactivity disorder: a resting-state functional magnetic resonance imaging study. Neuroreport 2006, 17:1033-1036.
18. Cordes D., Haughton V.M., Arfanakis K., Carew J.O., Turski P.A., Moritz C.H., Quigley M.A., Meyerand M.E. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. Am. J. Neuroradiol. 2001, 22:1326-1333.
19. Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam P.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13848-13853.
20. De L.M., Beckmann C.F., De S.N., Matthews P.M., Smith S.M. fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 2006, 29:1359-1367.
21. Destexhe A. Thalamic mechanisms for hypersynchorinized oscillations. Computational Neuroscience in Epilepsy 2008, 185-192. Academic Press, London. I. Soltesz, K. Staley (Eds.).
22. Erickson J.C., Clapp L.E., Ford G., Jabbari B. Somatosensory auras in refractory temporal lobe epilepsy. Epilepsia 2006, 47:202-206.
23. Fair D.A., Cohen A.L., Dosenbach N.U., Church J.A., Mietzin F.M., Barch D.M., Raichle M.E., Petersen S.E., Schlaggar B.L. The maturing architecture of the brain's default network. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4028-4032.
24. Fastenau P.S., Jianzhao S., Dunn D.W., Austin J.K. Academic underachievement among children with epilepsy: proportion exceeding psychometric criteria for learning disability and associated risk factors. J. Learn. Disabil. 2008, 41:195-207.
25. Finnish Version for International Classification of Diseases 10th Revision, 1999. National Institute for Health and Welfare, Helsinki.
26. Filippini N., MacIntosh B.J., Hough M.G., Goodwin G.M., Frisoni G.B., Smith S.M., Matthews P.M., Beckmann C.F., Mackay C.E. Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7209-7214.
27. Formisano E., Linden D.E., Di S.F., Trojano L., Esposito F., Sack A.T., Grossi P., Zanella F.E., Goebel R. Tracking the mind's image in the brain. I. Time-resolved fMRI during visuospatial mental imagery. Neuron 2002, 35:185-194.
28. Gao W., Zhu H., Giovanello K.S., Smith J.K., Shen D., Gilmore J.H., Lin W. Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6790-6795.
29. Garrity A.G., Pearlson G.D., McKiernan K., Lloyd D., Kiehl K.A., Calhoun V.D. Aberrant "default mode" functional connectivity in schizophrenia. Am. J. Psychiatry 2007, 164:450-457.
30. Good C., Johnsrude I., Ashburner J., Henson R., Friston K., Frackowiak R. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
31. Gotman J., Grova C., Bagshaw A., Kobayashi E., Aghakhani Y., Dubeau F. Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15236-15240.
32. Grant A.C. Interictal perceptual function in epilepsy. Epilepsy Behav. 2005, 6:511-519.
33. Grant A.C., Donnelly K.M., Chubb C., Barr W.B., Kuzniecky R., Devinsky O. Temporal lobe epilepsy does not impair visual perception. Epilepsia 2008, 49:710-713.
34. Grant A.C., Henry T.R., Fernandez R., Hill M.A., Sathian K. Somatosensory processing is impaired in temporal lobe epilepsy. Epilepsia 2005, 46:534-539.
35. Greicius M.D., Flores B.H., Menon V., Glover G.H., Solvason H.B., Kenna H., Reiss A.L., Schatzberg A.F. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 2007, 62:429-437.
36. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:253-258.
37. Greicius M.D., Srivastava G., Reiss A.L., Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2004, 1014:637-4642.
38. Greicius M.D., Kiviniemi V., Tervonen O., Vainionpää V., Alahuhta S., Reiss A.L., Menon V. Persistent default-mode network connectivity during light sedation. Hum. Brain Mapp. 2008, 29:839-847.
39. Gusnard D.A., Raichle M.E., Raichle M.E. Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2001, 2:685-694.
40. International League Against Epilepsy Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 1989, 30:389-399.
41. Jansen J.F.A., Aldenkamp A.P., Majoie H.J.M., Reijs R.P., de Krom M.C.T.F.M., Hofman P.A.M., Kooi M.E., Nicolay K., Backes W.H. Functional MRI reveals declined prefrontal cortex activation in patients with epilepsy on topiramate therapy. Epilepsy Behav. 2006, 1:181-185.
42. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
43. Kennedy D.P., Redcay E., Courchesne E. Failing to deactivate: resting functional abnormalities in autism. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8275-8280.
44. Killory B.D., Bai X., Negishi M., Vega C., Spann M.N., Vestal M., Guo J., Berman R., Danielson N., Trejo J., Shisler D., Novotny E.J., Constable T., Blumenfeld H. Impaired attention and network connectivity in childhood absence epilepsy. Neuroimage 2011, 56:2209-2217.
45. Kiviniemi V., Jauhiainen V., Tervonen O., Pääkkö E., Oikarinen J., Vainionpää V., Rantala H., Biswal B. Slow vasomotor fluctuation in fMRI of anesthetized child brain. Magn. Reson. Med. 2000, 44(3):373-378.
46. Kiviniemi V., Kantola J.H., Jauhiainen J., Hyvärinen A., Tervonen O. Independent component analysis of nondeterministic fMRI signal sources. Neuroimage 2003, 19:253-260.
47. Kiviniemi V.J., Haanpää H., Kantola J.H., Jauhiainen J., Vainionpää V., Alahuhta S., Tervonen O. Midazolam sedation increases fluctuation and synchrony of the resting brain BOLD signal. Magn. Reson. Imaging 2005, 23:531-537.
48. Kiviniemi V., Starck T., Remes J., Long X., Nikkinen J., Haapea M., Veijola J., Moilanen I., Isohanni M., Zang Y.F., Tervonen O. Functional segmentation of the brain cortex using high model order group PICA. Hum. Brain Mapp. 2009, 30:3865-3886.
49. Knecht S., Henningsen H., Deppe M., Osinska L., Diehl B., Stodieck S., Ringelstein E.B. Persistent unihemispheric perceptual impairments in humans following focal seizures. Neurosci. Lett. 1996, 217:66-68.
50. Kobayashi E., Bagshaw A.P., Grova C., Dubeau F., Gotman J. Negative BOLD responses to epileptic spikes. Hum. Brain Mapp. 2006, 27:488-497.
51. Laufs H., Hamandi K., Salek-Haddadi A., Kleinschmidt A.K., Duncan J.S., Lemieux L. Temporal lobe interictal epileptic discharges affect cerebral activity in "default mode" brain regions. Hum. Brain Mapp. 2007, 28:1023-1032.
52. Liao W., Zhang Z., Pan Z., Mantini D., Ding J., Duan X., Luo C., Luo G., Chen H. Altered functional connectivity and small-world in mesial temporal lobe epilepsy. PLoS One 2010, 5:e852.
53. Littow H., Elseoud A.A., Haapea M., Isohanni M., Moilanen I., Mankinen K., Nikkinen J., Rahko J., Rantala H., Remes J., Starck T., Tervonen O., Veijola J., Beckmann C., Kiviniemi V. Age-related differences in functional nodes of the brain cortex - a high model order group ICA study. Front. Syst. Neurosci. 2010, 4:1-11.
54. Liu Y., Liang M., Zhou Y., He Y., Hao Y., Song M., Yu C., Liu H., Liu Z., Jiang T. Disrupted small-world networks in schizophrenia. Brain 2008, 131:945-961.
55. Lowe M.J., Mock B.J., Sorenson J.A. Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 1998, 7:119-132.
56. Mankinen K., Long X.Y., Paakki J.J., Harila M., Rytky S., Tervonen O., Nikkinen J., Starck T., Remes J., Rantala H., Zang Y.F., Kiviniemi V. Alterations in regional homogeneity of baseline brain activity in pediatric temporal lobe epilepsy. Brain Res. 2011, 1373:221-229.
57. McKeown M.J., Makeig S., Brown G.G., Jung T.P., Kindermann S.S., Bell A.J., Sejnowski T.J. Analysis of fMRI data by blind separation into independent spatial components. Hum. Brain Mapp. 1998, 6:160-188.
58. Mitra P.P., Ogava S., Hu X., Ugurbil K. The nature of spatiotemporal changes in cerebral hemodynamics as manifested in functional magnetic resonance imaging. Magn. Reson. Med. 1997, 37:511-518.
59. Morgan V.L., Li Y., Abou-Khalil B., Gore J.C. Development of 2dTCA for the detection of irregular, transient BOLD activity. Hum. Brain Mapp. 2008, 29:57-69.
60. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
61. Paakki J.J., Rahko J., Long X., Moilanen I., Tervonen O., Nikkinen J., Starck T., Remes J., Hurtig T., Haapsamo H., Jussila K., Kuusikko-Gauffin S., Mattila M.L., Zang Y., Kiviniemi V. Alterations in regional homogeneity of resting-state brain activity in autism spectrum disorders. Brain Res. 2010, 1321:169-179.
62. Pizoli C.E., Shah M.N., Snyder A., Shimony J.S., Limbrick D.D., Raichle M.E., Schlaggar B.L., Syth M.D. Resting-state activity in development and maintenance of normal brain function. Proc. Natl. Acad. Sci. U. S. A. 2011, 28:11638-11643.
63. Rahko J.S., Paakki J.J., Starck T.H., Nikkinen J., Kätsyri J.V., Jansson-Verkasalo E.M., Carter A.S., Hurtig T.M., Mattila M.L., Remes J.J., Kuusikko-Gauffin S.A., Sams M.E., Bölte S., Ebeling H.E., Moilanen I.K., Tervonen O., Kiviniemi V. Valence scaling of dynamic facial expressions is altered in high-functioning subjects with autism spectrum disorders: an fMRI study. J. Autism Dev. Disord. 2011, (August 6, Epub).
64. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:676-682.
65. Rombouts S.A., Barkhof F., Goekoop R., Stam C.J., Scheltens P. Altered resting state networks in mild cognitive impairment and mild Alzheimer's disease: an fMRI study. Hum. Brain Mapp. 2005, 26:231-239.
66. Sack A.T., Camprodon J.A., Pascual-Leone A., Goebel R. The dynamics of interhemispheric compensatory processes in mental imagery. Science 2005, 308:702-704.
67. Sack A.T. Parietal cortex and spatial cognition. Behav. Brain Res. 2009, 202:153-161.
68. Sillanpää M., Jalava M., Kaleva O., Shinnar S. Long-term prognosis of seizures with onset in childhood. N. Engl. J. Med. 1998, 338:1715-1722.
69. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
70. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23:208-219.
71. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
72. Uddin L.Q., Kelly A.M., Biswal B.B., Margulies D.S., Shehzad Z., Shaw D., Ghaffari M., Rotrosen J., Adler L.A., Castellanos S.F., Milham M.P. Network homogeneity reveals decreased integrity of default-mode network in ADHD. J. Neurosci. Methods 2008, 169:249-254.
73. Vannucci M., Dietl T., Pezer N., Viggiano M.D., Helmstaedter C., Schaller C., Elger C.E., Grunwald T. Hippocampal function and visual object processing in temporal lobe epilepsy. Neuroreport 2003, 14:1489-1492.
74. Wechsler D. Wechsler Intelligence Scale for Children - III 1999, The Psychological Corporation, Sidcup, UK.
75. Weng S.J., Wiggins J.L., Peltier S.J., Carrasco M., Risi S., Lord C., Monk C.S. Alterations of resting state functional connectivity in the default network in adolescents with autism spectrum disorders. Brain Res. 2010, 1313:202-214.
76. Whitfield-Gabrieli S., Thermenos H.W., Milanovic S., Tsuang M.T., Faraone S.V., McCarley R.W., Shenton M.E., Green A.I., Nieto-Castanon A., LaViolette P., Wojcik J., Gabrieli J.D., Seidman L.J. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1279-1284.
77. Zhang Z., Lu G., Zhong Y., Tan Q., Liao W., Chen Z., Shi J., Liu Y. Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI. J. Neurol. 2009, 256:1705-1713.
78. Zhang Z., Lu G., Zhong Y., Tan Q., Liao W., Wang Z., Li K., Chen H., Liu Y. Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res. 2010, 1323:152-160.