Graph theoretical analysis reveals disrupted topological properties of whole brain functional networks in temporal lobe epilepsy

Clinical Neurophysiology

Volumn 125, Issue 9, 2014, Pages 1744-1756

  Wang, Junjing ^a   Qiu, Shijun ^b   Xu, Yong ^a   Liu, Zhenyin ^b   Wen, Xue ^a   Hu, Xiangshu ^c   Zhang, Ruibin ^a   Li, Meng ^a   Wang, Wensheng ^c   Huang, Ruiwang ^a  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

^c Guangdong 999 Brain Hospital   (China)

Author keywords

Duration of epilepsy; Efficiency; Functional networks; Graph theory

Indexed keywords

CARBAMAZEPINE;

ADULT; ANGULAR GYRUS; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE DURATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; INFERIOR FRONTAL GYRUS; MALE; MIDDLE TEMPORAL GYRUS; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE SCANNER; PARAHIPPOCAMPAL GYRUS; PARIETAL GYRUS; PRIORITY JOURNAL; SUPRAMARGINAL GYRUS; TEMPORAL LOBE EPILEPSY; THEORETICAL STUDY; BRAIN; BRAIN MAPPING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; YOUNG ADULT;

ADULT; BRAIN; BRAIN MAPPING; EPILEPSY, TEMPORAL LOBE; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; REPRODUCIBILITY OF RESULTS; YOUNG ADULT;

EID: 84906079750     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2013.12.120     Document Type: Article

References (92)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput Biol 2007, 3:e17.
2. Addis D.R., Moscovitch M., McAndrews M.P. Consequences of hippocampal damage across the autobiographical memory network in left temporal lobe epilepsy. Brain 2007, 130:2327-2342.
3. Ahmadi M.E., Hagler D.J., McDonald C.R., Tecoma E.S., Iragui V.J., Dale A.M., et al. Side matters: diffusion tensor imaging tractography in left and right temporal lobe epilepsy. AJNR Am J Neuroradiol 2009, 30:1740-1747.
4. Akanuma N., Alarcon G., Lum F., Kissani N., Koutroumanidis M., Adachi N., et al. Lateralising value of neuropsychological protocols for presurgical assessment of temporal lobe epilepsy. Epilepsia 2003, 44:408-418.
5. Akanuma N., Reed L.J., Marsden P.K., Jarosz J., Adachi N., Hallett W.A., et al. Hemisphere-specific episodic memory networks in the human brain: a correlation study between intracarotid amobarbital test and [(18)F]FDG-PET. J Cogn Neurosci 2009, 21:605-622.
6. Akman C.I., Ichise M., Olsavsky A., Tikofsky R.S., Van Heertum R.L., Gilliam F. Epilepsy duration impacts on brain glucose metabolism in temporal lobe epilepsy: results of voxel-based mapping. Epilepsy Behav 2010, 17:373-380.
7. Anand A., Li Y., Wang Y., Lowe M.J., Dzemidzic M. Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression. Psychiatry Res 2009, 171:189-198.
8. Bartolomei F., Bettus G., Stam C.J., Guye M. Interictal network properties in mesial temporal lobe epilepsy: a graph theoretical study from intracerebral recordings. Clin Neurophysiol 2013, 124:2345-2353.
9. Bassett D.S., Bullmore E. Small-world brain networks. Neuroscientist 2006, 12:512-523.
10. Bell B., Lin J.J., Seidenberg M., Hermann B. The neurobiology of cognitive disorders in temporal lobe epilepsy. Nat Rev Neurol 2011, 7:154-164.
11. Bernhardt B.C., Rozen D.A., Worsley K.J., Evans A.C., Bernasconi N., Bernasconi A. Thalamo-cortical network pathology in idiopathic generalized epilepsy: insights from MRI-based morphometric correlation analysis. NeuroImage 2009, 46:373-381.
12. Bernhardt B.C., Chen Z., He Y., Evans A.C., Bernasconi N. Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb Cortex 2011, 21:2147-2157.
13. Bernhardt B.C., Bernasconi N., Kim H., Bernasconi A. Mapping thalamocortical network pathology in temporal lobe epilepsy. Neurology 2012, 78:129-136.
14. Bettus G., Guedj E., Joyeux F., Confort-Gouny S., Soulier E., Laguitton V., et al. Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms. Hum Brain Mapp 2009, 30:1580-1591.
15. Bonilha L., Rorden C., Castellano G., Pereira F., Rio P.A., Cendes F., et al. Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Arch Neurol - Chicago 2004, 61:1379-1384.
16. Braun U., Plichta M.M., Esslinger C., Sauer C., Haddad L., Grimm O., et al. Test-retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures. NeuroImage 2012, 59:1404-1412.
17. Brazdil M., Chlebus P., Mikl M., Pazourkova M., Krupa P., Rektor I. Reorganization of language-related neuronal networks in patients with left temporal lobe epilepsy - an fMRI study. Eur J Neurol 2005, 12:268-275.
18. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009, 10:186-198.
19. Bullmore E.T., Suckling J., Overmeyer S., Rabe-Hesketh S., Taylor E., Brammer M.J. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 1999, 18:32-42.
20. Cabeza R., Nyberg L. Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci 2000, 12:1-47.
21. Chao L.L., Haxby J.V., Martin A. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nat Neurosci 1999, 2:913-919.
22. Cohen J. A power primer. Psychol Bull 1992, 112:155-159.
23. Craddock R.C., Jbabdi S., Yan C.-G., Vogelstein J.T., Castellanos F.X., Di Martino A., et al. Imaging human connectomes at the macroscale. Nat Methods 2013, 10:524-539.
24. de Reus M.A., van den Heuvel M.P. The parcellation-based connectome: limitations and extensions. NeuroImage 2013, 80:397-404.
25. de Vico Fallani F., Astolfi L., Cincotti F., Mattia D., Marciani M.G., Salinari S., et al. Cortical functional connectivity networks in normal and spinal cord injured patients: evaluation by graph analysis. Hum Brain Mapp 2007, 28:1334-1346.
26. Dosenbach N.U.F., Nardos B., Cohen A.L., Fair D.A., Power J.D., Church J.A., et al. Prediction of individual brain maturity using fMRI. Science 2010, 329:1358-1361.
27. Doucet G., Osipowicz K., Sharan A., Sperling M.R., Tracy J.I. Extratemporal functional connectivity impairments at rest are related to memory performance in mesial temporal epilepsy. Hum Brain Mapp 2013, 34:2202-2216.
28. Edefonti V., Bravi F., Turner K., Beghi E., Canevini M.P., Ferraroni M., et al. Health-related quality of life in adults with epilepsy: the effect of age, age at onset and duration of epilepsy in a multicentre Italian study. BMC Neurol 2011, 11:33.
29. Ferrier C.H., Alarcon G., Glover A., Koutroumanidis M., Morris R.G., Simmons A., et al. N-acetylaspartate and creatine levels measured by (1)H MRS relate to recognition memory. Neurology 2000, 55:1874-1883.
30. Fornito A., Zalesky A., Bullmore E.T. Network scaling effects in graph analytic studies of human resting-state FMRI data. Front Syst Neurosci 2010, 4:22.
31. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. PNAS 2005, 102:9673-9678.
32. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 2009, 101:3270-3283.
33. Greicius M. Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 2008, 21:424-430.
34. Gupta V.K., Singh A.K., Gupta B. Development of membrane electrodes for selective determination of some antiepileptic drugs in pharmaceuticals, plasma and urine. Anal Bioanal Chem 2007, 389:2019-2028.
35. Guye M., Regis J., Tamura M., Wendling F., McGonigal A., Chauvel P., et al. The role of corticothalamic coupling in human temporal lobe epilepsy. Brain 2006, 129:1917-1928.
36. Haneef Z., Lenartowicz A., Yeh H.J., Engel J., Stern J.M. Effect of lateralized temporal lobe epilepsy on the default mode network. Epilepsy Behav 2012, 25:350-357.
37. He Y., Evans A. Graph theoretical modeling of brain connectivity. Curr Opin Neurol 2010, 23:341-350.
38. He Y., Chen Z., Evans A. Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J Neurosci 2008, 28:4756-4766.
39. He Y., Dagher A., Chen Z., Charil A., Zijdenbos A., Worsley K., et al. Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. Brain 2009, 132:3366-3379.
40. Heim S., Opitz B., Friederici A.D. Broca's area in the human brain is involved in the selection of grammatical gender for language production: evidence from event-related functional magnetic resonance imaging. Neurosci Lett 2002, 328:101-104.
41. Hermann B.P., Seidenberg M., Haltiner A., Wyler A.R. Adequacy of language function and verbal memory performance in unilateral temporal lobe epilepsy. Cortex 1992, 28:423-433.
42. Holmes M., Folley B.S., Sonmezturk H.H., Gore J.C., Kang H., Abou-Khalil B., et al. Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy. Hum Brain Mapp 2014, 35:735-744.
43. Humphries M.D., Gurney K., Prescott T.J. The brainstem reticular formation is a small-world, not scale-free, network. Proc Biol Sci 2006, 273:503-511.
44. ILAE 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.
45. Jensen E.J., Hargreaves I., Bass A., Pexman P., Goodyear B.G., Federico P. Cortical reorganization and reduced efficiency of visual word recognition in right temporal lobe epilepsy: a functional MRI study. Epilepsy Res 2011, 93:155-163.
46. Kennedy D.N., Lange N., Makris N., Bates J., Meyer J., Caviness V.S. Gyri of the human neocortex: an MRI-based analysis of volume and variance. Cereb Cortex 1998, 8:372-384.
47. Lacruz M.E., Garcia Seoane J.J., Valentin A., Selway R., Alarcon G. Frontal and temporal functional connections of the living human brain. Eur J Neurol 2007, 26:1357-1370.
48. Lambon Ralph M.A., Cipolotti L., Manes F., Patterson K. Taking both sides: do unilateral anterior temporal lobe lesions disrupt semantic memory?. Brain 2010, 133:3243-3255.
49. Lambon Ralph M.A., Ehsan S., Baker G.A., Rogers T.T. Semantic memory is impaired in patients with unilateral anterior temporal lobe resection for temporal lobe epilepsy. Brain 2012, 135:242-258.
50. Liao W., Zhang Z., Pan Z., Mantini D., Ding J., Duan X., et al. Altered functional connectivity and small-world in mesial temporal lobe epilepsy. Plos One 2010, 5:e8525.
51. Liao W., Zhang Z., Pan Z., Mantini D., Ding J., Duan X., et al. Default mode network abnormalities in mesial temporal lobe epilepsy: a study combining fMRI and DTI. Hum Brain Mapp 2011, 32:883-895.
52. Liu Y., Liang M., Zhou Y., He Y., Hao Y., Song M., et al. Disrupted small-world networks in schizophrenia. Brain 2008, 131:945-961.
53. 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.
54. Lynall M.E., Bassett D.S., Kerwin R., McKenna P.J., Kitzbichler M., Muller U., et al. Functional connectivity and brain networks in schizophrenia. J Neurosci 2010, 30:9477-9487.
55. Maguire E.A., Vargha-Khadem F., Mishkin M. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 2001, 124:1156-1170.
56. Mayeux R., Brandt J., Rosen J., Benson D.F. Interictal memory and language impairment in temporal lobe epilepsy. Neurology 1980, 30:120-125.
57. McDonald C.R., Ahmadi M.E., Hagler D.J., Tecoma E.S., Iragui V.J., Gharapetian L., et al. Diffusion tensor imaging correlates of memory and language impairments in temporal lobe epilepsy. Neurology 2008, 71:1869-1876.
58. Morgan V.L., Gore J.C., Abou-Khalil B. Functional epileptic network in left mesial temporal lobe epilepsy detected using resting fMRI. Epilepsy Res 2010, 88:168-178.
59. Pail M., Brazdil M., Marecek R., Mikl M. An optimized voxel-based morphometric study of gray matter changes in patients with left-sided and right-sided mesial temporal lobe epilepsy and hippocampal sclerosis (MTLE/HS). Epilepsia 2010, 51:511-518.
60. Pereira F.R., Alessio A., Sercheli M.S., Pedro T., Bilevicius E., Rondina J.M., et al. Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI. BMC Neurosci 2010, 11:66.
61. Ponten S.C., Bartolomei F., Stam C.J. Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 2007, 118:918-927.
62. Powell H.W.R., Richardson M.P., Symms M.R., Boulby P.A., Thompson P.J., Duncan J.S., et al. Reorganization of verbal and nonverbal memory in temporal lobe epilepsy due to unilateral hippocampal sclerosis. Epilepsia 2007, 48:1512-1525.
63. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. NeuroImage 2010, 52:1059-1069.
64. Seeck M. Epilepsy: repeat MRI in patients with chronic epilepsy. Nat Rev Neurol 2013, 9:545-546.
65. Seghier M.L. The angular gyrus: multiple functions and multiple subdivisions. Neuroscientist 2013, 19:43-61.
66. Sidhu M.K., Stretton J., Winston G.P., Bonelli S., Centeno M., Vollmar C., et al. A functional magnetic resonance imaging study mapping the episodic memory encoding network in temporal lobe epilepsy. Brain 2013, 136:1868-1888.
67. Sporns O., Honey C.J. Small worlds inside big brains. Proc Natl Acad Sci USA 2006, 103:19219-19220.
68. Stretton J., Winston G., Sidhu M., Centeno M., Vollmar C., Bonelli S., et al. Neural correlates of working memory in temporal lobe epilepsy - an fMRI study. NeuroImage 2012, 60:1696-1703.
69. Supekar K., Menon V., Rubin D., Musen M., Greicius M.D. Network analysis of intrinsic functional brain connectivity in Alzheimer's disease. PLoS Comput Biol 2008, 4:e1000100.
70. Thivard L., Hombrouck J., du Montcel S.T., Delmaire C., Cohen L., Samson S., et al. Productive and perceptive language reorganization in temporal lobe epilepsy. NeuroImage 2005, 24:841-851.
71. Tian L., Wang J., Yan C., He Y. Hemisphere- and gender-related differences in small-world brain networks: a resting-state functional MRI study. NeuroImage 2011, 54:191-202.
72. Tranel D., Damasio H., Damasio A.R. A neural basis for the retrieval of conceptual knowledge. Neuropsychologia 1997, 35:1319-1327.
73. Triantafyllou C., Hoge R.D., Krueger G., Wiggins C.J., Potthast A., Wiggins G.C., et al. Comparison of physiological noise at 1.5T, 3T and 7T and optimization of fMRI acquisition parameters. NeuroImage 2005, 26:243-250.
74. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15:273-289.
75. Ugurbil K., Toth L., Kim D.S. How accurate is magnetic resonance imaging of brain function?. Trends Neurosci 2003, 26:108-114.
76. van Dellen E., Douw L., Baayen J.C., Heimans J.J., Ponten S.C., Vandertop W.P., et al. Long-term effects of temporal lobe epilepsy on local neural networks: a graph theoretical analysis of corticography recordings. Plos One 2009, 4.
77. van den Heuvel M.P., Hulshoff Pol H.E. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 2010, 20:519-534.
78. Vlooswijk M.C., Vaessen M.J., Jansen J.F., de Krom M.C., Majoie H.J., Hofman P.A., et al. Loss of network efficiency associated with cognitive decline in chronic epilepsy. Neurology 2011, 77:938-944.
79. Voets N.L., Adcock J.E., Stacey R., Hart Y., Carpenter K., Matthews P.M., et al. Functional and structural changes in the memory network associated with left temporal lobe epilepsy. Hum Brain Mapp 2009, 30:4070-4081.
80. Voets N.L., Beckmann C.F., Cole D.M., Hong S., Bernasconi A., Bernasconi N. Structural substrates for resting network disruption in temporal lobe epilepsy. Brain 2012, 135:2350-2357.
81. Waites A.B., Briellmann R.S., Saling M.M., Abbott D.F., Jackson G.D. Functional connectivity networks are disrupted in left temporal lobe epilepsy. Ann Neurol 2006, 59:335-343.
82. Wang J., Wang L., Zang Y., Yang H., Tang H., Gong Q., et al. Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Hum Brain Mapp 2009, 30:1511-1523.
83. Wang L., Zhu C., He Y., Zang Y., Cao Q., Zhang H., et al. Altered small-world brain functional networks in children with attention-deficit/hyperactivity disorder. Hum Brain Mapp 2009, 30:638-649.
84. Wang J.H., Zuo X.N., Gohel S., Milham M.P., Biswal B.B., He Y. Graph theoretical analysis of functional brain networks: test-retest evaluation on short- and long-term resting-state functional MRI data. Plos One 2011, 6:e21976.
85. Watkins K., Paus T. Modulation of motor excitability during speech perception: the role of Broca's area. J Cogn Neurosci 2004, 16:978-987.
86. Watts D.J., Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 1998, 393:440-442.
87. Yan C., Zang Y. DPARSF: A MATLAB toolbox for "Pipeline" data analysis of resting-state fMRI. Front Syst Neurosci 2010, 4:13.
88. Zhang Z., Lu G., Zhong Y., Tan Q., Liao W., Chen Z., et al. Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI. J Neurol 2009, 256:1705-1713.
89. Zhang Z., Lu G., Zhong Y., Tan Q., Yang Z., Liao W., et al. Impaired attention network in temporal lobe epilepsy: a resting FMRI study. Neurosci Lett 2009, 458:97-101.
90. Zhang Z., Lu G., Zhong Y., Tan Q., Liao W., Wang Z., et al. Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res 2010, 1323:152-160.
91. Zhang Z., Liao W., Chen H., Mantini D., Ding J.R., Xu Q., et al. Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain 2011, 134:2912-2928.
92. Zheng J.N., Qin B.L., Dang C., Ye W., Chen Z.R., Yu L. Alertness network in patients with temporal lobe epilepsy: a fMRI study. Epilepsy Res 2012, 100:67-73.