Structural connectivity differences in left and right temporal lobe epilepsy

NeuroImage

Volumn 100, Issue , 2014, Pages 135-144

  Besson, Pierre ^a   Dinkelacker, Vera ^b,c,d   Valabregue, Romain ^c,d   Thivard, Lionel ^d   Leclerc, Xavier ^a   Baulac, Michel ^b,d   Sammler, Daniela ^c,e   Colliot, Olivier ^d,f   Lehéricy, Stéphane ^c,d   Samson, Séverine ^b,g   Dupont, Sophie ^b,c,d  

^a LILLE UNIVERSITY HOSPITAL   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c Centre de NeuroImagerie de Recherche (CENIR)   (France)

^d SORBONNE UNIVERSITÉ   (France)

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

^f INRIA ROCQUENCOURT   (France)

^g UNIV LILLE   (France)

Author keywords

Connectivity; Connectome; Hippocampal sclerosis; Network based statistics; Temporal lobe epilepsy

Indexed keywords

ADULT; ANATOMIC LANDMARK; ANATOMICAL VARIATION; ARTICLE; BRAIN MAPPING; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; FEMALE; FRACTIONAL ANISOTROPY; HEMISPHERIC DOMINANCE; HIPPOCAMPAL SCLEROSIS; HUMAN; IMAGE ANALYSIS; INTERMETHOD COMPARISON; MALE; NERVE CELL NETWORK; NEUROANATOMY; NEUROIMAGING; NEUROPHYSIOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; TEMPORAL LOBE EPILEPSY; WHITE MATTER; COMPLICATION; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SCLEROSIS;

ADULT; CONNECTOME; EPILEPSY, TEMPORAL LOBE; FEMALE; FUNCTIONAL LATERALITY; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; SCLEROSIS;

EID: 84903886540     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.04.071     Document Type: Article

References (73)

1. 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(9):1740-1747. (Epub 2009/06/11).
2. Behrens T.E., Berg H.J., Jbabdi S., Rushworth M.F., Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?. NeuroImage 2007, 34(1):144-155.
3. Behrens T.E., Johansen-Berg H., Woolrich M.W., Smith S.M., Wheeler-Kingshott C.A., Boulby P.A., et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 2003, 6(7):750-757. (Epub 2003/06/17).
4. Benjamini Y., Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 2001, 29(4):1165-1188.
5. Bernasconi N., Duchesne S., Janke A., Lerch J., Collins D.L., Bernasconi A. Whole-brain voxel-based statistical analysis of gray matter and white matter in temporal lobe epilepsy. NeuroImage 2004, 23(2):717-723.
6. Bernhardt B.C., Bernasconi N., Concha L., Bernasconi A. Cortical thickness analysis in temporal lobe epilepsy: reproducibility and relation to outcome. Neurology 2010, 74(22):1776-1784. (Epub 2010/06/02).
7. 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(9):2147-2157. (Epub 2011/02/19).
8. Bernhardt B.C., Hong S., Bernasconi A., Bernasconi N. Imaging structural and functional brain networks in temporal lobe epilepsy. Front. Hum. Neurosci. 2013, 7:624.
9. Bernhardt B.C., Worsley K.J., Besson P., Concha L., Lerch J.P., Evans A.C., et al. Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: insights on the relation between mesiotemporal connectivity and cortical atrophy. NeuroImage 2008, 42(2):515-524. (Epub 2008/06/17).
10. 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(5):1580-1591. (Epub 2008/07/29).
11. Bettus G., Wendling F., Guye M., Valton L., Regis J., Chauvel P., et al. Enhanced EEG functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res. 2008, 81(1):58-68. (Epub 2008/06/13).
12. Bonilha L., Alessio A., Rorden C., Baylis G., Damasceno B.P., Min L.L., et al. Extrahippocampal gray matter atrophy and memory impairment in patients with medial temporal lobe epilepsy. Hum. Brain Mapp. 2007, 28(12):1376-1390.
13. Bonilha L., Edwards J.C., Kinsman S.L., Morgan P.S., Fridriksson J., Rorden C., et al. Extrahippocampal gray matter loss and hippocampal deafferentation in patients with temporal lobe epilepsy. Epilepsia 2010, 51(4):519-528. (Epub 2010/02/19).
14. Bonilha L., Helpern J.A., Sainju R., Nesland T., Edwards J.C., Glazier S.S., et al. Presurgical connectome and postsurgical seizure control in temporal lobe epilepsy. Neurology 2013, 81(19):1704-1710.
15. Bonilha L., Nesland T., Martz G.U., Joseph J.E., Spampinato M.V., Edwards J.C., et al. Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures. J. Neurol. Neurosurg. Psychiatry 2012, 83(9):903-909.
16. Buchel C., Raedler T., Sommer M., Sach M., Weiller C., Koch M.A. White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb. Cortex 2004, 14(9):945-951. (Epub 2004/04/30).
17. Coan A.C., Appenzeller S., Bonilha L., Li L.M., Cendes F. Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy. Neurology 2009, 73(11):834-842.
18. Concha L., Beaulieu C., Gross D.W. Bilateral limbic diffusion abnormalities in unilateral temporal lobe epilepsy. Ann. Neurol. 2005, 57(2):188-196. (Epub 2004/11/25).
19. Concha L., Kim H., Bernasconi A., Bernhardt B.C., Bernasconi N. Spatial patterns of water diffusion along white matter tracts in temporal lobe epilepsy. Neurology 2012, 79(5):455-462.
20. Cormack F., Cross J.H., Isaacs E., Harkness W., Wright I., Vargha-Khadem F., et al. The development of intellectual abilities in pediatric temporal lobe epilepsy. Epilepsia 2007, 48(1):201-204. (Epub 2007/01/24).
21. Diehl B., Busch R.M., Duncan J.S., Piao Z., Tkach J., Luders H.O. Abnormalities in diffusion tensor imaging of the uncinate fasciculus relate to reduced memory in temporal lobe epilepsy. Epilepsia 2008, 49(8):1409-1418. (Epub 2008/04/10).
22. Dupont S., Ottaviani M., Thivard L., Semah F., Samson Y., Baulac M. Temporal pole hypometabolism may be linked to a reduction of grey matter in temporal lobe epilepsy. Neuroreport 2002, 13(18):2537-2541.
23. Dupont S., Tanguy M.L., Clemenceau S., Adam C., Hazemann P., Baulac M. Long-term prognosis and psychosocial outcomes after surgery for MTLE. Epilepsia 2006, 47(12):2115-2124. (Epub 2007/01/05).
24. Engel J., Thompson P.M., Stern J.M., Staba R.J., Bragin A., Mody I. Connectomics and epilepsy. Curr. Opin. Neurol. 2013, 26(2):186-194.
25. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33(3):341-355. (Epub 2002/02/08).
26. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Segonne F., Salat D.H., et al. Automatically parcellating the human cerebral cortex. Cereb. Cortex 2004, 14(1):11-22. (Epub 2003/12/05).
27. Focke N.K., Yogarajah M., Bonelli S.B., Bartlett P.A., Symms M.R., Duncan J.S. Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. NeuroImage 2008, 40(2):728-737.
28. Fonov V., Evans A.C., Botteron K., Almli C.R., McKinstry R.C., Collins D.L. Unbiased average age-appropriate atlases for pediatric studies. NeuroImage 2011, 54(1):313-327.
29. Frisk V., Milner B. The role of the left hippocampal region in the acquisition and retention of story content. Neuropsychologia 1990, 28(4):349-359.
30. Glasser M.F., Rilling J.K. DTI tractography of the human brain's language pathways. Cereb. Cortex 2008, 18(11):2471-2482. (Epub 2008/02/19).
31. Gleissner U., Helmstaedter C., Schramm J., Elger C.E. Memory outcome after selective amygdalohippocampectomy in patients with temporal lobe epilepsy: one-year follow-up. Epilepsia 2004, 45(8):960-962. (Epub 2004/07/24).
32. Gleissner U., Helmstaedter C., Schramm J., Elger C.E. Memory outcome after selective amygdalohippocampectomy: a study in 140 patients with temporal lobe epilepsy. Epilepsia 2002, 43(1):87-95. (Epub 2002/03/07).
33. Govindan R.M., Makki M.I., Sundaram S.K., Juhasz C., Chugani H.T. Diffusion tensor analysis of temporal and extra-temporal lobe tracts in temporal lobe epilepsy. Epilepsy Res. 2008, 80(1):30-41. (Epub 2008/04/26).
34. Gross D.W. Diffusion tensor imaging in temporal lobe epilepsy. Epilepsia 2011, 52(Suppl. 4):32-34. (Epub 2011/07/16).
35. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., et al. Mapping the structural core of human cerebral cortex. PLoS Biol. 2008, 6(7):e159. (Epub 2008/07/04).
36. Haneef Z., Lenartowicz A., Yeh H.J., Levin H.S., Engel J., Stern J.M. Functional connectivity of hippocampal networks in temporal lobe epilepsy. Epilepsia 2014, 55(1):137-145.
37. Jeurissen B., Leemans A., Tournier J.D., Jones D.K., Sijbers J. Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum. Brain Mapp. 2013, 34(11):2747-2766.
38. Jokeit H., Seitz R.J., Markowitsch H.J., Neumann N., Witte O.W., Ebner A. Prefrontal asymmetric interictal glucose hypometabolism and cognitive impairment in patients with temporal lobe epilepsy. Brain 1997, 120(Pt 12):2283-2294.
39. Jones D.K., Knosche T.R., Turner R. White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. NeuroImage 2013, 73:239-254.
40. Keller S.S., Schoene-Bake J.-C., Gerdes J.S., Weber B., Deppe M. Concomitant Fractional Anisotropy and Volumetric Abnormalities in Temporal Lobe Epilepsy: Cross-Sectional Evidence for Progressive Neurologic Injury. PLoS One 2012, 7(10):e46791.
41. Keller S.S., Wieshmann U.C., Mackay C.E., Denby C.E., Webb J., Roberts N. Voxel based morphometry of grey matter abnormalities in patients with medically intractable temporal lobe epilepsy: effects of side of seizure onset and epilepsy duration. J. Neurol. Neurosurg. Psychiatry 2002, 73(6):648-656.
42. Kemmotsu N., Girard H.M., Bernhardt B.C., Bonilha L., Lin J.J., Tecoma E.S., et al. MRI analysis in temporal lobe epilepsy: cortical thinning and white matter disruptions are related to side of seizure onset. Epilepsia 2011, 52(12):2257-2266. (Epub 2011/10/07).
43. Kim H., Bernasconi N., Bernhardt B., Colliot O., Bernasconi A. Basal temporal sulcal morphology in healthy controls and patients with temporal lobe epilepsy. Neurology 2008, 70(22):2159-2165.
44. Kim H., Mansi T., Bernasconi N. Disentangling hippocampal shape anomalies in epilepsy. Front. Neurol. 2013, 4:131. (Epub 2013/09/26).
45. Kucukboyaci N.E., Girard H.M., Hagler D.J., Kuperman J., Tecoma E.S., Iragui V.J., et al. Role of frontotemporal fiber tract integrity in task-switching performance of healthy controls and patients with temporal lobe epilepsy. J. Int. Neuropsychol. Soc. 2012, 18(1):57-67. (Epub 2011/10/22).
46. Lebel C., Beaulieu C. Lateralization of the arcuate fasciculus from childhood to adulthood and its relation to cognitive abilities in children. Hum. Brain Mapp. 2009, 30(11):3563-3573. (Epub 2009/04/15).
47. Lee C.Y., Tabesh A., Benitez A., Helpern J.A., Jensen J.H., Bonilha L. Microstructural integrity of early-versus late-myelinating white matter tracts in medial temporal lobe epilepsy. Epilepsia 2013, 54(10):1801-1809.
48. Liu M., Concha L., Lebel C., Beaulieu C., Gross D.W. Mesial temporal sclerosis is linked with more widespread white matter changes in temporal lobe epilepsy. NeuroImage 2012, 1(1):99-105.
49. 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(23):1869-1876. (Epub 2008/10/24).
50. Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clin. Neurosurg. 1972, 19:421-446.
51. Mullaart R.A., Daniels O., Hopman J.C., deHaan A.F., Stoelinga G.B., Rotteveel J.J. Rotteveel JJ. Asymmetry of the cerebral blood flow: An ultrasound Doppler study in preterm newborns. Pediatr. Neurol. 1995, 13(4):319-322.
52. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9(1):97-113.
53. Oostrom K.J., Smeets-Schouten A., Kruitwagen C.L.J.J., Peters A.C.B., Jennekens-Schinkel A. Childhood ftDSGoEi. Not Only a Matter of Epilepsy: Early Problems of Cognition and Behavior in Children With "Epilepsy Only"-A Prospective, Longitudinal, Controlled Study Starting at Diagnosis. Pediatrics 2003, 112(6):1338-1344.
54. Otte W.M., van Eijsden P., Sander J.W., Duncan J.S., Dijkhuizen R.M., Braun K.P.J. A meta-analysis of white matter changes in temporal lobe epilepsy as studied with diffusion tensor imaging. Epilepsia 2012, 53(4):659-667.
55. Powell H.W., Parker G.J., Alexander D.C., Symms M.R., Boulby P.A., Barker G.J., et al. Imaging language pathways predicts postoperative naming deficits. J. Neurol. Neurosurg. Psychiatry 2008, 79(3):327-330. (Epub 2007/11/17).
56. Richardson M. Brain networks in human epilepsy. J. Neurol. Neurosurg. Psychiatry 2013, 84(9):e1.
57. Riederer F., Lanzenberger R., Kaya M., Prayer D., Serles W., Baumgartner C. Network atrophy in temporal lobe epilepsy: a voxel-based morphometry study. Neurology 2008, 71(6):419-425.
58. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. NeuroImage 2010, 52(3):1059-1069. (Epub 2009/10/13).
59. Semah F., Baulac M., Hasboun D., Frouin V., Mangin J.F., Papageorgiou S., et al. Is Interictal Temporal Hypometabolism Related to Mesial Temporal Sclerosis - a Positron Emission Tomography Magnetic-Resonance-Imaging Confrontation. Epilepsia 1995, 36(5):447-456.
60. Smith M.L., Milner B. Right hippocampal impairment in the recall of spatial location: Encoding deficit or rapid forgetting?. Neuropsychologia 1989, 27(1):71-81.
61. Sporns O., Zwi J.D. The small world of the cerebral cortex. Neuroinformatics 2004, 2(2):145-162. (Epub 2004/08/21).
62. Stretton J., Thompson P.J. Frontal lobe function in temporal lobe epilepsy. Epilepsy Res. 2012, 98(1):1-13.
63. 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(3):841-851. (Epub 2005/01/18).
64. Thivard L., Lehericy S., Krainik A., Adam C., Dormont D., Chiras J., et al. Diffusion tensor imaging in medial temporal lobe epilepsy with hippocampal sclerosis. NeuroImage 2005, 28(3):682-690.
65. Tournier J.D., Calamante F., Connelly A. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 2007, 35(4):1459-1472. (Epub 2007/03/24).
66. Vernooij M.W., Smits M., Wielopolski P.A., Houston G.C., Krestin G.P., van der Lugt A. Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: A combined fMRI and DTI study. NeuroImage 2007, 35(3):1064-1076.
67. Verstraete E., Veldink J.H., Mandl R.C., van den Berg L.H., van den Heuvel M.P. Impaired structural motor connectome in amyotrophic lateral sclerosis. PLoS One 2011, 6(9):e24239. (Epub 2011/09/14).
68. Vlooswijk M.C., Jansen J.F., Majoie H.J., Hofman P.A., de Krom M.C., Aldenkamp A.P., et al. Functional connectivity and language impairment in cryptogenic localization-related epilepsy. Neurology 2010, 75(5):395-402. (Epub 2010/08/04).
69. Wieser H.G., Ortega M., Friedman A., Yonekawa Y. Long-term seizure outcomes following amygdalohippocampectomy. J. Neurosurg. 2003, 98(4):751-763. (Epub 2003/04/15).
70. Yogarajah M., Powell H.W.R., Parker G.J.M., Alexander D.C., Thompson P.J., Symms M.R., et al. Tractography of the parahippocampal gyrus and material specific memory impairment in unilateral temporal lobe epilepsy. NeuroImage 2008, 40(4):1755-1764.
71. Zalesky A., Cocchi L., Fornito A., Murray M.M., Bullmore E. Connectivity differences in brain networks. NeuroImage 2012, 60(2):1055-1062.
72. Zalesky A., Fornito A., Bullmore E.T. Network-based statistic: identifying differences in brain networks. NeuroImage 2010, 53(4):1197-1207. (Epub 2010/07/06).
73. Zalesky A., Fornito A., Seal M.L., Cocchi L., Westin C.F., Bullmore E.T., et al. Disrupted Axonal Fiber Connectivity in Schizophrenia. Biol. Psychiatry 2011, 69(1):80-89.