Subregional mesiotemporal network topology is altered in temporal lobe epilepsy

Cerebral Cortex

Volumn 26, Issue 7, 2016, Pages 3237-3248

  Bernhardt, Boris C ^a,b   Bernasconi, Neda ^a   Hong, Seok Jun ^a   Dery, Sebastian ^a   Bernasconi, Andrea ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

Author keywords

Connectivity; Epilepsy; Graph theory; MRI; Temporal lobe

Indexed keywords

ADOLESCENT; ADULT; AMYGDALA; ARTICLE; AXON; CONTROLLED STUDY; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; HUMAN; LIMBIC CORTEX; MAJOR CLINICAL STUDY; MALE; MORPHOMETRICS; NERVE CELL NETWORK; NERVE SPROUTING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROGNOSIS; REPRODUCIBILITY; SUBREGIONAL MESIOTEMPORAL NETWORK; TEMPORAL LOBE EPILEPSY; AGED; DIAGNOSTIC IMAGING; DRUG RESISTANT EPILEPSY; FOLLOW UP; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; MIDDLE AGED; NERVE TRACT; TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AMYGDALA; DRUG RESISTANT EPILEPSY; ENTORHINAL CORTEX; EPILEPSY, TEMPORAL LOBE; FEMALE; FOLLOW-UP STUDIES; FUNCTIONAL LATERALITY; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84981289256     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv166     Document Type: Article

References (71)

1. Achard S, Bullmore E. 2007. Efficiency and cost of economical brain functional networks. PLoS Comput Biol. 3:e17.
2. Adler DH, Pluta J, Kadivar S, Craige C, Gee JC, Avants BB, Yushkevich PA. 2014. Histology-derived volumetric annotation of the human hippocampal subfields in postmortem MRI. Neuroimage. 84:505-523.
3. Alexander-Bloch A, Giedd JN, Bullmore E. 2013. Imaging structural co-variance between human brain regions. Nat Neurosci. 14:322-336.
4. Alexander-Bloch A, Raznahan A, Bullmore E, Giedd J. 2013. The convergence of maturational change and structural covariance in human cortical networks. J Neurosci. 33:2889-2899.
5. Amunts K, Kedo O, Kindler M, Pieperhoff P, Mohlberg H, Shah NJ, Habel U, Schneider F, Zilles K. 2005. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat Embryol. 210:343-352.
6. Bartolomei F, Bettus G, Stam CJ, Guye M. 2013. Interictal network properties in mesial temporal lobe epilepsy: a graph theoretical study from intracerebral recordings. Clin Neurophysiol. 124:2345-2353.
7. Bellec P, Rosa-Neto P, Lyttelton OC, Benali H, Evans AC. 2010. Multi-level bootstrap analysis of stable clusters in restingstate fMRI. Neuroimage. 51:1126-1139.
8. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 57:289-300.
9. Bernasconi N, Bernasconi A, Andermann F, Dubeau F, FeindelW, Reutens DC. 1999. Entorhinal cortex in temporal lobe epilepsy: a quantitative MRI study. Neurology. 52:1870-1876.
10. Bernasconi N, Bernasconi A, Caramanos Z, Antel SB, Andermann F, Arnold DL. 2003. Mesial temporal damage in temporal lobe epilepsy: a volumetric MRI study of the hippocampus, amygdala and parahippocampal region. Brain. 126:462-469.
11. Bernhardt BC, Bernasconi N, Kim H, Bernasconi A. 2012. Mapping thalamocortical network pathology in temporal lobe epilepsy. Neurology. 78:129-136.
12. Bernhardt BC, Chen Z, He Y, Evans AC, Bernasconi N. 2011. Graphtheoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb Cortex. 21:2147-2157.
13. Bernhardt BC, Hong S, Bernasconi A, Bernasconi N. 2013. Imaging structural and functional brain networks in temporal lobe epilepsy. Front Hum Neurosci. 7:624.
14. Bernhardt BC, Hong SJ, Bernasconi A, Bernasconi N. 2015. Magnetic resonance imaging pattern learning in temporal lobe epilepsy: classification and prognostics. Ann Neurol. 77(3):436-446.
15. Bernhardt BC, Kim H, Bernasconi N. 2013. Patterns of subregional mesiotemporal disease progression in temporal lobe epilepsy. Neurology. 81:1840-1847.
16. Bernhardt BC, Worsley KJ, Besson P, Concha L, Lerch JP, Evans AC, Bernasconi N. 2008. Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: insights on the relation between mesiotemporal connectivity and cortical atrophy. Neuroimage. 42:515-524.
17. Bettus G, Guedj E, Joyeux F, Confort-Gouny S, Soulier E, Laguitton V, Cozzone PJ, Chauvel P, Ranjeva JP, Bartolomei F, et al. 2009. Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms. Hum Brain Mapp. 30:1580-1591.
18. Blondel VD, Guillaume JL, Lambiotte R, Lefebre E. 2008. Fast unfolding of communities in large networks. J Stat Mech Theory Exp. P10008.
19. Blumcke I, Beck H, Lie AA, Wiestler OD. 1999. Molecular neuropathology of human mesial temporal lobe epilepsy. Epilepsy Res. 36:205-223.
20. Blumcke I, Thom M, Aronica E, Armstrong DD, Bartolomei F, Bernasconi A, Bernasconi N, Bien CG, Cendes F, Coras R, et al. 2013. International consensus classification of hippocampal sclerosis in temporal lobe epilepsy: a Task Force report from the ILAE Commission on Diagnostic Methods. Epilepsia. 54 (7):1315-1329.
21. Bonilha L, Edwards JC, Kinsman SL, Morgan PS, Fridriksson J, Rorden C, Rumboldt Z, Roberts DR, Eckert MA, Halford JJ. 2010. Extrahippocampal gray matter loss and hippocampal deafferentation in patients with temporal lobe epilepsy. Epilepsia. 51:519-528.
22. Bonilha L, Helpern JA, Sainju R, Nesland T, Edwards JC, Glazier SS, Tabesh A. 2013. Presurgical connectome and postsurgical seizure control in temporal lobe epilepsy. Neurology. 81:1704-1710.
23. Bonilha L, Nesland T, Martz GU, Joseph JE, Spampinato MV, Edwards JC, Tabesh A. 2012. Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures. J Neurol Neurosurg Psychiatry. 83:903-909.
24. Bonilha L, Rorden C, Halford JJ, Eckert M, Appenzeller S, Cendes F, Li LM. 2007. Asymmetrical extra-hippocampal grey matter loss related to hippocampal atrophy in patients with medial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 78:286-294.
25. Bragin A, Wilson CL, Engel J Jr. 2000. Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia. 41(Suppl 6): S144-S152.
26. Bullmore E, Sporns O. 2009. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Neurosci. 10:186-198.
27. Cammoun L, Gigandet X, Meskaldji D, Thiran JP, Sporns O, Do KQ, Maeder P, Meuli R, Hagmann P. 2012. Mapping the human connectome at multiple scales with diffusion spectrum MRI. J Neurosci Methods. 203:386-397.
28. Cavazos JE, Zhang P, Qazi R, Sutula TP. 2003. Ultrastructural features of sprouted mossy fiber synapses in kindled and kainic acid-treated rats. J Comp Neurol. 458:272-292.
29. Collins DL, Neelin P, Peters TM, Evans AC. 1994. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr. 18:192-205.
30. Concha L, Beaulieu C, Gross DW. 2005. Bilateral limbic diffusion abnormalities in unilateral temporal lobe epilepsy. Ann Neurol. 57:188-196.
31. Concha L, Livy DJ, Beaulieu C, Wheatley BM, Gross DW. 2010. In vivo diffusion tensor imaging and histopathology of the fimbria-fornix in temporal lobe epilepsy. J Neurosci. 30:996-1002.
32. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD. 1989. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 495:387-395.
33. Duvernoy HM. 2005. The human hippocampus functional anatomy, vascularization and serial sections with MRI. 3rd ed. Berlin, Heidelberg: Springer.
34. Dyhrfjeld-Johnsen J, Santhakumar V, Morgan RJ, Huerta R, Tsimring L, Soltesz I. 2007. Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysiol. 97:1566-1587.
35. Engel J Jr, Van Ness PC, Rasmussen T, Ojemann LM. 1993. Outcome with respect to epileptic seizures. In: Engel J Jr. Surgical treatment of the epilepsies. New York: Raven. 609-621.
36. Gerig G, Styner M, Jones D, Weinberg DR, LiebermanJ. 2001. Shape analysis of brain ventricles using SPHARM. MMBIA 171-178. doi:10. 1109/MMBIA. 2001. 991731.
37. Gong G, He Y, Chen ZJ, Evans AC. 2012. Convergence and divergence of thickness correlations with diffusion connections across the human cerebral cortex. Neuroimage. 59:1239-1248.
38. He Y, Chen ZJ, Evans AC. 2007. Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex. 17:2407-2419.
39. He Y, Chen Z, Evans A. 2008. Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J Neurosci. 28:4756-4766.
40. He Y, Wang J, Wang L, Chen ZJ, Yan C, Yang H, Tang H, Zhu C, Gong Q, Zang Y, et al. 2009. Uncovering intrinsic modular organization of spontaneous brain activity in humans. PLoS One. 4:e5226.
41. Hogan RE, Moseley ED, Maccotta L. 2015. Hippocampal surface deformation accuracy in t1-weighted volumetric MRI sequences in subjects with epilepsy. J Neuroimaging. 25:452-459.
42. Hogan RE, Wang L, Bertrand ME, Willmore LJ, Bucholz RD, Nassif AS, Csernansky JG. 2004. MRI-based high-dimensional hippocampal mapping in mesial temporal lobe epilepsy. Brain. 127:1731-1740.
43. Holmes M, Folley BS, Sonmezturk HH, Gore JC, Kang H, Abou-Khalil B, Morgan VL. 2014. Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy. Hum Brain Mapp. 35:735-744.
44. Hosseini SM, Kesler SR. 2013. Comparing connectivity pattern and small-world organization between structural correlation and resting-state networks in healthy adults. Neuroimage. 78:402-414.
45. Insausti R, Tuñón T, Sobreviela T, Insausti AM, Gonzalo LM. 1995. The human entorhinal cortex: a cytoarchitectonic analysis. J Comp Neurol. 355:171-198.
46. Kelly C, Toro R, Di Martino A, Cox CL, Bellec P, Castellanos FX, Milham MP. 2012. A convergent functional architecture of the insula emerges across imaging modalities. Neuroimage. 61:1129-1142.
47. Kemmotsu N, Kucukboyaci NE, Cheng CE, Girard HM, Tecoma ES, Iragui VJ, McDonald CR. 2013. Alterations in functional connectivity between the hippocampus and prefrontal cortex as a correlate of depressive symptoms in temporal lobe epilepsy. Epilepsy Behav. 29:552-559.
48. KimH, Besson P, Colliot O, Bernasconi A, Bernasconi N. 2008. Surface-based vector analysis using heat equation interpolation: a newapproach to quantify local hippocampal volume changes. Med Image Comput Comput Assist Interv. 11:1008-1015.
49. Knopp A, Kivi A, Wozny C, Heinemann U, Behr J. 2005. Cellular and network properties of the subiculum in the pilocarpine model of temporal lobe epilepsy. J Comp Neurol. 483:476-488.
50. Kramer MA, Kolaczyk ED, Kirsch HE. 2008. Emergent network topology at seizure onset in humans. Epilepsy Res. 79:173-186.
51. Kucukboyaci NE, Kemmotsu N, Cheng CE, Girard HM, Tecoma ES, Iragui VJ, McDonald CR. 2013. Functional connectivity of the hippocampus in temporal lobe epilepsy: feasibility of a taskregressed seed-based approach. Brain Connect. 3:464-474.
52. Latora V, Marchiori M. 2001. Efficient behavior of small-world networks. Phys Rev Lett. 87:198701.
53. Liao W, Zhang Z, Pan Z, Mantini D, Ding J, Duan X, Luo C, Lu G, Chen H. 2010. Altered functional connectivity and smallworld in mesial temporal lobe epilepsy. PLoS One. 5:e8525.
54. Maccotta L, Moseley ED, Benzinger TL, Hogan RE. 2015. Beyond the CA1 subfield: local hippocampal shape changes in MRInegative temporal lobe epilepsy. Epilepsia. 56(5):780-788.
55. Maslov S, Sneppen K. 2002. Specificity and stability in topology of protein networks. Science. 296:910-913.
56. Mathern GW, Babb TL, Leite JP, Pretorius K, Yeoman KM, Kuhlman PA. 1996. The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Res. 26:151-161.
57. Mueller SG, Laxer KD, Barakos J, Cheong I, Finlay D, Garcia P, Cardenas-Nicolson V, Weiner MW. 2009. Involvement of the thalamocortical network in TLE with and without mesiotemporal sclerosis. Epilepsia. 46(2):353-359.
58. Newman ME. 2003. The structure and function of complex networks. SIAM Rev Soc Ind Appl Math. 45:167-256.
59. Otte WM, Dijkhuizen RM, van Meer MP, van der Hel WS, Verlinde SA, van Nieuwenhuizen O, Viergever MA, Stam CJ, Braun KP. 2012. Characterization of functional and structural integrity in experimental focal epilepsy: reduced network efficiency coincides with white matter changes. PLoS One. 7: e39078.
60. Pittau F, Grova C, Moeller F, Dubeau F, Gotman J. 2012. Patterns of altered functional connectivity in mesial temporal lobe epilepsy. Epilepsia. 53:1013-1023.
61. Ponten SC, Bartolomei F, Stam CJ. 2007. Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol. 118:918-927.
62. Schindler KA, Bialonski S, Horstmann MT, Elger CE, Lehnertz K. 2008. Evolving functional network properties and synchronizability during human epileptic seizures. Chaos. 18:033119.
63. Sled JG, Zijdenbos AP, Evans AC. 1998. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging. 17:87-97.
64. Sporns O. 2011. The human connectome: a complex network. Ann N Y Acad Sci. 1224:109-125.
65. Sporns O, Zwi JD. 2004. The small world of the cerebral cortex. Neuroinformatics. 2:145-162.
66. Stretton J, Winston GP, Sidhu M, Bonelli S, Centeno M, Vollmar C, Cleary RA, Williams E, Symms MR, Koepp MJ, et al. 2013. Disrupted segregation of working memory networks in temporal lobe epilepsy. Neuroimage Clin. 2:273-281.
67. Styner M, Oguz I, Brechbuehler C, Pantazis D, Ger G. 2006. Statistical Shape Analysis of Brain Structures using SPHARM-PDM. In: MICCAI OpenSource Workshop. Copenhagen, Denmark.
68. Sutula T. 2002. Seizure-induced axonal sprouting: assessing connections between injury, local circuits, and epileptogenesis. Epilepsy Curr. 2:86-91.
69. Wang J, Qiu S, Xu Y, Liu Z, Wen X, Hu X, Zhang R, Li M, Wang W, Huang R. 2014. Graph theoretical analysis reveals disrupted topological properties of whole brain functional networks in temporal lobe epilepsy. Clin Neurophysiol. 125(9):1744-1756.
70. Watson C, Andermann F, Gloor P, Jones-Gotman M, Peters T, Evans A, Olivier A, Melanson D, Leroux G. 1992. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology. 42:1743-1750.
71. Watts DJ, Strogatz SH. 1998. Collective dynamics of 'small-world' networks. Nature. 393:440-442.