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Epilepsia. 2021 Dec;62(12):2941-2954. doi: 10.1111/epi.17098. Epub 2021 Oct 12.

Decoupling of functional and structural language networks in temporal lobe epilepsy.

Epilepsia

Karin Trimmel, Sjoerd B Vos, Lorenzo Caciagli, Fenglai Xiao, Louis A van Graan, Gavin P Winston, Matthias J Koepp, Pamela J Thompson, John S Duncan

Affiliations

  1. Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.
  2. Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, Queen Square, London, UK.
  3. Department of Neurology, Medical University of Vienna, Vienna, Austria.
  4. Centre for Medical Image Computing, University College London, London, UK.
  5. Neuroradiological Academic Unit, UCL Queen Square Institute of Neurology, University College London, London, UK.
  6. Department of Neurology, West China of Sichuan University, Chengdu, China.
  7. Division of Neurology, Department of Medicine, Queen's University, Kingston, Canada.

PMID: 34642939 DOI: 10.1111/epi.17098

Abstract

OBJECTIVE: To identify functional and structural alterations in language networks of people with temporal lobe epilepsy (TLE), who frequently present with naming and word-finding difficulties.

METHODS: Fifty-five patients with unilateral TLE (29 left) and 16 controls were studied with auditory and picture naming functional magnetic resonance imaging (fMRI) tasks. Activation maxima in the left posterobasal temporal lobe were used as seed regions for whole-brain functional connectivity analyses (psychophysiological interaction). White matter language pathways were investigated using diffusion tensor imaging and neurite orientation dispersion and density imaging metrics extracted along fiber bundles starting from fMRI-guided seeds. Regression analyses were performed to investigate the correlation of functional connectivity with diffusion MRI metrics.

RESULTS: In the whole group of patients and controls, weaker functional connectivity from the left posterobasal temporal lobe (1) to the bilateral anterior temporal lobe, precentral gyrus, and lingual gyrus during auditory naming and (2) to the bilateral occipital cortex and right fusiform gyrus during picture naming was associated with decreased neurite orientation dispersion and higher free water fraction of white matter tracts. Compared to controls, TLE patients exhibited fewer structural connections and an impaired coupling of functional and structural metrics.

SIGNIFICANCE: TLE is associated with an impairment and decoupling of functional and structural language networks. White matter damage, as evidenced by diffusion abnormalities, may contribute to impaired functional connectivity and language dysfunction in TLE.

© 2021 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.

Keywords: DTI; NODDI; diffusion MRI; functional connectivity; language network; naming function; temporal lobe epilepsy

References

  1. Davey D, Thompson P. Interictal language functioning in chronic epilepsy. J Neurolinguistics. 1991;6:381-99. - PubMed
  2. Trimmel K, Caciagli L, Xiao F, van Graan LA, Koepp MJ, Thompson PJ, et al. Impaired naming performance in temporal lobe epilepsy: language fMRI responses are modulated by disease characteristics. J Neurol. 2020;268:147-60. - PubMed
  3. Trimmel K, van Graan AL, Caciagli L, Haag A, Koepp MJ, Thompson PJ, et al. Left temporal lobe language network connectivity in temporal lobe epilepsy. Brain. 2018;141:2406-18. - PubMed
  4. Powell HWR, Parker GJM, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CAM, et al. Abnormalities of language networks in temporal lobe epilepsy. Neuroimage. 2007;36:209-21. - PubMed
  5. Powell HWR, Parker GJM, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CAM, et al. Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage. 2006;32:388-99. - PubMed
  6. Gonzálvez GG, Trimmel K, Haag A, van Graan LA, Koepp MJ, Thompson PJ, et al. Activations in temporal areas using visual and auditory naming stimuli: a language fMRI study in temporal lobe epilepsy. Epilepsy Res. 2016;128:102-12. - PubMed
  7. Trimmel K, Graan LA, Gonzálvez GG, Haag A, Caciagli L, Vos SB, et al. Naming fMRI predicts the effect of temporal lobe resection on language decline. Ann Clin Transl Neurol. 2019;6:2186-96. - PubMed
  8. Fonseca A-D, Guedj E, Alario F-X, Laguitton V, Mundler O, Chauvel P, et al. Brain regions underlying word finding difficulties in temporal lobe epilepsy. Brain. 2009;132:2772-84. - PubMed
  9. McDonald CR, Ahmadi ME, Hagler DJ, Tecoma ES, Iragui VJ, Gharapetian L, et al. Diffusion tensor imaging correlates of memory and language impairments in temporal lobe epilepsy. Neurology. 2008;71:1869-76. - PubMed
  10. Leroux E, Delcroix N, Dollfus S. Left fronto-temporal dysconnectivity within the language network in schizophrenia: an fMRI and DTI study. Psychiatry Res. 2014;223:261-7. - PubMed
  11. Winston GP. The physical and biological basis of quantitative parameters derived from diffusion MRI. Quant Imaging Med Surg. 2012;2:254-65. - PubMed
  12. Winston GP, Vos SB, Caldairou B, Hong S-J, Czech M, Wood TC, et al. Microstructural imaging in temporal lobe epilepsy: diffusion imaging changes relate to reduced neurite density. Neuroimage Clin. 2020;26:102231. - PubMed
  13. Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC. NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage. 2012;61:1000-16. - PubMed
  14. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97-113. - PubMed
  15. McKenna P, Warrington E. Graded naming test: manual. Windsor, UK: NFER-Nelson Publishing Co; 1983. - PubMed
  16. Nelson HE, Wilson J. National adult reading test (NART). Windsor, UK: NFER-Nelson Publishing Co; 1991. - PubMed
  17. Friston KJ, Holmes AP, Worsley KJ, Poline J-P, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp. 1995;2:189-210. - PubMed
  18. Wilke M, Lidzba K. LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods. 2007;163:128-36. - PubMed
  19. Caciagli L, Allen LA, He X, Trimmel K, Vos SB, Centeno M, et al. Thalamus and focal to bilateral seizures: a multiscale cognitive imaging study. Neurology. 2020;95:e2427-41. - PubMed
  20. Friston KJ. Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp. 1994;2:56-78. - PubMed
  21. Vos SB, Tax CMW, Luijten PR, Ourselin S, Leemans A, Froeling M. The importance of correcting for signal drift in diffusion MRI. Magn Reson Med. 2017;77:285-99. - PubMed
  22. Andersson JLR, Skare S, Ashburner J. How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage. 2003;20:870-88. - PubMed
  23. Andersson JLR, Sotiropoulos SN. An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage. 2016;125:1063-78. - PubMed
  24. Cardoso MJ, Modat M, Wolz R, Melbourne A, Cash D, Rueckert D, et al. Geodesic information flows: spatially-variant graphs and their application to segmentation and fusion. IEEE Trans Med Imaging. 2015;34:1976-88. - PubMed
  25. Smith RE, Tournier J-D, Calamante F, Connelly A. Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage. 2012;62:1924-38. - PubMed
  26. Tournier J-D, Smith R, Raffelt D, Tabbara R, Dhollander T, Pietsch M, et al. MRtrix3: a fast, flexible and open software framework for medical image processing and visualisation. Neuroimage. 2019;202:116137. - PubMed
  27. Ciccarelli O, Parker G, Toosy AT, Wheeler-Kingshott C, Barker GJ, Boulby PA, et al. From diffusion tractography to quantitative white matter tract measures: a reproducibility study. Neuroimage. 2003;18:348-59. - PubMed
  28. Wandschneider B, Burdett J, Townsend L, Hill A, Thompson PJ, Duncan JS, et al. Effect of topiramate and zonisamide on fMRI cognitive networks. Neurology. 2017;88:1165-71. - PubMed
  29. Xiao F, Caciagli L, Wandschneider B, Sander JW, Sidhu M, Winston G, et al. Effects of carbamazepine and lamotrigine on functional magnetic resonance imaging cognitive networks. Epilepsia. 2018;59:1362-71. - PubMed
  30. Yasuda CL, Centeno M, Vollmar C, Stretton J, Symms M, Cendes F, et al. The effect of topiramate on cognitive fMRI. Epilepsy Res. 2013;105:250-5. - PubMed
  31. Middlebrooks EH, Yagmurlu K, Szaflarski JP, Rahman M, Bozkurt B. A contemporary framework of language processing in the human brain in the context of preoperative and intraoperative language mapping. Neuroradiology. 2017;59:69-87. - PubMed
  32. Winston GP, Daga P, White MJ, Micallef C, Miserocchi A, Mancini L, et al. Preventing visual field deficits from neurosurgery. Neurology. 2014;83:604-11. - PubMed
  33. Mancini M, Vos SB, Vakharia VN, O'Keeffe AG, Trimmel K, Barkhof F, et al. Automated fiber tract reconstruction for surgery planning: extensive validation in language-related white matter tracts. Neuroimage Clin. 2019;23:101883. - PubMed
  34. Alexander AL, Hasan KM, Lazar M, Tsuruda JS, Parker DL. Analysis of partial volume effects in diffusion-tensor MRI. Magn Reson Med. 2001;45:770-80. - PubMed
  35. Sone D, Sato N, Ota M, Maikusa N, Kimura Y, Matsuda H. Abnormal neurite density and orientation dispersion in unilateral temporal lobe epilepsy detected by advanced diffusion imaging. Neuroimage Clin. 2018;20:772-82. - PubMed
  36. Thom M. Hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol. 2014;40:520-43. - PubMed
  37. Batalle D, O'Muircheartaigh J, Makropoulos A, Kelly CJ, Dimitrova R, Hughes EJ, et al. Different patterns of cortical maturation before and after 38 weeks gestational age demonstrated by diffusion MRI in vivo. Neuroimage. 2019;185:764-75. - PubMed
  38. Kamiya K, Hori M, Aoki S. NODDI in clinical research. J Neurosci Methods. 2020;346:108908. - PubMed
  39. Takaya S, Liu H, Greve DN, Tanaka N, Leveroni C, Cole AJ, et al. Altered anterior-posterior connectivity through the arcuate fasciculus in temporal lobe epilepsy. Hum Brain Mapp. 2016;37:4425-38. - PubMed
  40. Caciagli L, Bernasconi A, Wiebe S, Koepp MJ, Bernasconi N, Bernhardt BC. A meta-analysis on progressive atrophy in intractable temporal lobe epilepsy: time is brain? Neurology. 2017;89:506-16. - PubMed
  41. Wang W-H, Liou H-H, Chen C-C, Chiu M-J, Chen T-F, Cheng T-W, et al. Neuropsychological performance and seizure-related risk factors in patients with temporal lobe epilepsy: a retrospective cross-sectional study. Epilepsy Behav. 2011;22:728-34. - PubMed
  42. Hamberger MJ, Seidel WT, Goodman RR, Williams A, Perrine K, Devinsky O, et al. Evidence for cortical reorganization of language in patients with hippocampal sclerosis. Brain J Neurol. 2007;130:2942-50. - PubMed
  43. Foesleitner O, Nenning K-H, Bartha-Doering L, Baumgartner C, Pataraia E, Moser D, et al. Lesion-specific language network alterations in temporal lobe epilepsy. AJNR Am J Neuroradiol. 2020;41:147-54. - PubMed
  44. Koubeissi M. Resting connectivity in non-lesional temporal lobe epilepsy. Epilepsy Curr. 2017;17:219-20. - PubMed
  45. Davies KG, Bell BD, Bush AJ, Hermann BP, Dohan FC, Jaap AS. Naming decline after left anterior temporal lobectomy correlates with pathological status of resected hippocampus. Epilepsia. 1998;39:407-19. - PubMed
  46. Hermann BP, Perrine K, Chelune GJ, Barr W, Loring DW, Strauss E, et al. Visual confrontation naming following left anterior temporal lobectomy: a comparison of surgical approaches. Neuropsychology. 1999;13:3-9. - PubMed
  47. Bell BD, Seidenberg M, Hermann BP, Douville K. Visual and auditory naming in patients with left or bilateral temporal lobe epilepsy. Epilepsy Res. 2003;55:29-37. - PubMed
  48. Westin C-F, Knutsson H, Pasternak O, Szczepankiewicz F, Özarslan E, van Westen D, et al. Q-space trajectory imaging for multidimensional diffusion MRI of the human brain. Neuroimage. 2016;135:345-62. - PubMed

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