دورية أكاديمية
Naming fMRI-guided white matter language tract volumes influence naming decline after temporal lobe resection.
| العنوان: | Naming fMRI-guided white matter language tract volumes influence naming decline after temporal lobe resection. |
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| المؤلفون: | Trimmel K; Department of Neurology, Medical University of Vienna, Vienna, Austria. k.trimmel@ucl.ac.uk.; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK. k.trimmel@ucl.ac.uk.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK. k.trimmel@ucl.ac.uk., Vos SB; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK.; Neuroradiological Academic Unit, UCL Queen Square Institute of Neurology, London, UK.; Centre for Microscopy Characterisation and Analysis, University of Western Australia, Nedlands, Australia., Binding L; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK.; Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK., Caciagli L; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK.; Department of Neurology, Inselspital, Sleep-Wake-Epilepsy-Center, Bern University Hospital, University of Bern, Bern, Switzerland., Xiao F; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK., van Graan LA; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK., Koepp MJ; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK., Thompson PJ; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK., Duncan JS; Epilepsy Society MRI Unit, Epilepsy Society, Chalfont St Peter, UK.; Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, UK. |
| المصدر: | Journal of neurology [J Neurol] 2024 Jul; Vol. 271 (7), pp. 4158-4167. Date of Electronic Publication: 2024 Apr 07. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 0423161 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-1459 (Electronic) Linking ISSN: 03405354 NLM ISO Abbreviation: J Neurol Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Berlin ; New York, Springer-Verlag |
| مواضيع طبية MeSH: | White Matter*/diagnostic imaging , White Matter*/surgery , Magnetic Resonance Imaging* , Epilepsy, Temporal Lobe*/surgery , Epilepsy, Temporal Lobe*/diagnostic imaging , Epilepsy, Temporal Lobe*/physiopathology , Temporal Lobe*/surgery , Temporal Lobe*/diagnostic imaging , Temporal Lobe*/physiopathology, Humans ; Male ; Female ; Adult ; Middle Aged ; Diffusion Tensor Imaging ; Young Adult ; Language Disorders/etiology ; Language Disorders/diagnostic imaging ; Language Disorders/physiopathology ; Functional Laterality/physiology ; Postoperative Complications/diagnostic imaging ; Postoperative Complications/etiology ; Postoperative Complications/physiopathology ; Language ; Neural Pathways/diagnostic imaging ; Neural Pathways/physiopathology ; Neural Pathways/surgery |
| مستخلص: | Objective: The aim of this study was to explore the relation of language functional MRI (fMRI)-guided tractography with postsurgical naming decline in people with temporal lobe epilepsy (TLE). Methods: Twenty patients with unilateral TLE (9 left) were studied with auditory and picture naming functional MRI tasks. Activation maxima in the left posterobasal temporal lobe were used as seed regions for whole-brain fibre tractography. Clinical naming performance was assessed preoperatively, 4 months, and 12 months following temporal lobe resection. Volumes of white matter language tracts in both hemispheres as well as tract volume laterality indices were explored as moderators of postoperative naming decline using Pearson correlations and multiple linear regression with other clinical variables. Results: Larger volumes of white matter language tracts derived from auditory and picture naming maxima in the hemisphere of subsequent surgery as well as stronger lateralization of picture naming tract volumes to the side of surgery correlated with greater language decline, which was independent of fMRI lateralization status. Multiple regression for picture naming tract volumes was associated with a significant decline of naming function with 100% sensitivity and 93% specificity at both short-term and long-term follow-up. Interpretation: Naming fMRI-guided white matter language tract volumes relate to postoperative naming decline after temporal lobe resection in people with TLE. This can assist stratification of surgical outcome and minimize risk of postoperative language deficits in TLE. (© 2024. The Author(s).) |
| References: | de Tisi J, Bell GS, Peacock JL et al (2011) The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet 378:1388–1395. https://doi.org/10.1016/S0140-6736(11)60890-8. (PMID: 10.1016/S0140-6736(11)60890-822000136) Davies KG, Bell BD, Bush AJ et al (1998) Naming decline after left anterior temporal lobectomy correlates with pathological status of resected hippocampus. Epilepsia 39:407–419. (PMID: 10.1111/j.1528-1157.1998.tb01393.x9578031) Sherman EMS, Wiebe S, Fay-McClymont TB et al (2011) Neuropsychological outcomes after epilepsy surgery: systematic review and pooled estimates: cognitive Change after Epilepsy Surgery. Epilepsia 52:857–869. https://doi.org/10.1111/j.1528-1167.2011.03022.x. (PMID: 10.1111/j.1528-1167.2011.03022.x21426331) Bonelli SB, Thompson PJ, Yogarajah M et al (2012) Imaging language networks before and after anterior temporal lobe resection: results of a longitudinal fMRI study. Epilepsia 53:639–650. https://doi.org/10.1111/j.1528-1167.2012.03433.x. (PMID: 10.1111/j.1528-1167.2012.03433.x224290734471632) Binder JR, Tong J-Q, Pillay SB et al (2020) Temporal lobe regions essential for preserved picture naming after left temporal epilepsy surgery. Epilepsia 61:1939–1948. https://doi.org/10.1111/epi.16643. (PMID: 10.1111/epi.16643327808787722029) Gross WL, Helfand AI, Swanson SJ et al (2022) Prediction of naming outcome With fMRI language lateralization in left temporal epilepsy surgery. Neurology 98:e2337–e2346. https://doi.org/10.1212/WNL.0000000000200552. (PMID: 10.1212/WNL.0000000000200552354109039202528) Busch RM, Floden DP, Prayson B et al (2016) Estimating risk of word-finding problems in adults undergoing epilepsy surgery. Neurology 87:2363–2369. https://doi.org/10.1212/WNL.0000000000003378. (PMID: 10.1212/WNL.0000000000003378278154065135025) Binding LP, Dasgupta D, Taylor PN et al (2023) Contribution of white matter fiber bundle damage to language change after surgery for temporal lobe epilepsy. Neurology 100:e1621–e1633. https://doi.org/10.1212/WNL.0000000000206862. (PMID: 10.1212/WNL.00000000002068623675038610103113) Hamberger MJ, Miozzo M, Schevon CA et al (2016) Functional differences among stimulation-identified cortical naming sites in the temporal region. Epilepsy Behav 60:124–129. https://doi.org/10.1016/j.yebeh.2016.04.021. (PMID: 10.1016/j.yebeh.2016.04.021272062304912888) Trimmel K, van Graan LA, Caciagli L et al (2018) Left temporal lobe language network connectivity in temporal lobe epilepsy. Brain 141:2406–2418. https://doi.org/10.1093/brain/awy164. (PMID: 10.1093/brain/awy16429939211) Gonzálvez GG, Trimmel K, Haag A et al (2016) Activations in temporal areas using visual and auditory naming stimuli: a language fMRI study in temporal lobe epilepsy. Epilepsy Res 128:102–112. https://doi.org/10.1016/j.eplepsyres.2016.10.009. (PMID: 10.1016/j.eplepsyres.2016.10.00927833066) Tracy JI (2022) fMRI has added value in predicting naming after epilepsy surgery. Neurology 98:959–960. https://doi.org/10.1212/WNL.0000000000200328. (PMID: 10.1212/WNL.000000000020032835410901) Trimmel K, Graan LA, Gonzálvez GG et al (2019) Naming fMRI predicts the effect of temporal lobe resection on language decline. Ann Clin Transl Neurol. https://doi.org/10.1002/acn3.50911. (PMID: 10.1002/acn3.50911315788196856622) Davies KG, Risse GL, Gates JR (2005) Naming ability after tailored left temporal resection with extraoperative language mapping: increased risk of decline with later epilepsy onset age. Epilepsy Behav EB 7:273–278. https://doi.org/10.1016/j.yebeh.2005.05.016. (PMID: 10.1016/j.yebeh.2005.05.016) Cervenka MC, Corines J, Boatman-Reich DF et al (2013) Electrocorticographic functional mapping identifies human cortex critical for auditory and visual naming. Neuroimage 69:267–276. https://doi.org/10.1016/j.neuroimage.2012.12.037. (PMID: 10.1016/j.neuroimage.2012.12.03723274183) Powell HW, Parker GJ, Alexander DC et al (2007) Abnormalities of language networks in temporal lobe epilepsy. Neuroimage 36:209–221. https://doi.org/10.1016/j.neuroimage.2007.02.028. (PMID: 10.1016/j.neuroimage.2007.02.02817400477) McDonald CR, Ahmadi ME, Hagler DJ et al (2008) Diffusion tensor imaging correlates of memory and language impairments in temporal lobe epilepsy. Neurology 71:1869–1876. https://doi.org/10.1212/01.wnl.0000327824.05348.3b. (PMID: 10.1212/01.wnl.0000327824.05348.3b189460012676974) Kaestner E, Stasenko A, Ben-Haim S et al (2022) The importance of basal-temporal white matter to pre- and post-surgical naming ability in temporal lobe epilepsy. NeuroImage Clin 34:102963. https://doi.org/10.1016/j.nicl.2022.102963. (PMID: 10.1016/j.nicl.2022.102963352201068888987) Powell HW, Parker GJ, Alexander DC et al (2008) Imaging language pathways predicts postoperative naming deficits. J Neurol Neurosurg Psychiatry 79:327–330. https://doi.org/10.1136/jnnp.2007.126078. (PMID: 10.1136/jnnp.2007.12607818006653) Trimmel K, Vos SB, Caciagli L et al (2021) Decoupling of functional and structural language networks in temporal lobe epilepsy. Epilepsia 62:2941–2954. https://doi.org/10.1111/epi.17098. (PMID: 10.1111/epi.17098346429398776336) Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. (PMID: 10.1016/0028-3932(71)90067-45146491) Friston KJ, Holmes AP, Worsley KJ et al (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210. (PMID: 10.1002/hbm.460020402) Wilke M, Lidzba K (2007) LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods 163:128–136. https://doi.org/10.1016/j.jneumeth.2007.01.026. (PMID: 10.1016/j.jneumeth.2007.01.02617386945) Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19:1233–1239. (PMID: 10.1016/S1053-8119(03)00169-112880848) Vos SB, Tax CMW, Luijten PR et al (2017) The importance of correcting for signal drift in diffusion MRI. Magn Reson Med 77:285–299. https://doi.org/10.1002/mrm.26124. (PMID: 10.1002/mrm.2612426822700) Andersson JLR, Skare S, Ashburner J (2003) How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. Neuroimage 20:870–888. https://doi.org/10.1016/S1053-8119(03)00336-7. (PMID: 10.1016/S1053-8119(03)00336-714568458) Andersson JLR, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125:1063–1078. https://doi.org/10.1016/j.neuroimage.2015.10.019. (PMID: 10.1016/j.neuroimage.2015.10.01926481672) Cardoso MJ, Modat M, Wolz R et al (2015) Geodesic information flows: spatially-variant graphs and their application to segmentation and fusion. IEEE Trans Med Imaging 34:1976–1988. https://doi.org/10.1109/TMI.2015.2418298. (PMID: 10.1109/TMI.2015.241829825879909) Smith RE, Tournier J-D, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62:1924–1938. https://doi.org/10.1016/j.neuroimage.2012.06.005. (PMID: 10.1016/j.neuroimage.2012.06.00522705374) Tournier J-D, Smith R, Raffelt D et al (2019) MRtrix3: a fast, flexible and open software framework for medical image processing and visualisation. Neuroimage 202:116137. https://doi.org/10.1016/j.neuroimage.2019.116137. (PMID: 10.1016/j.neuroimage.2019.11613731473352) Trimmel K, Caciagli L, Xiao F et al (2020) Impaired naming performance in temporal lobe epilepsy: language fMRI responses are modulated by disease characteristics. J Neurol. https://doi.org/10.1007/s00415-020-10116-x. (PMID: 10.1007/s00415-020-10116-x327479797815622) Powell HW, Parker GJ, Alexander DC et al (2006) Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage 32:388–399. https://doi.org/10.1016/j.neuroimage.2006.03.011. (PMID: 10.1016/j.neuroimage.2006.03.01116632380) Iglesias JE (2023) EasyReg: a ready-to-use deep learning tool for symmetric affine and nonlinear brain MRI registration. In Review. McKenna P, Warrington E (1983) Graded Naming Test: manual. NFER-Nelson Publishing Co, England. Thivard L, Hombrouck J, du Montcel ST et al (2005) Productive and perceptive language reorganization in temporal lobe epilepsy. Neuroimage 24:841–851. https://doi.org/10.1016/j.neuroimage.2004.10.001. (PMID: 10.1016/j.neuroimage.2004.10.00115652319) Crow AJD, Thomas A, Rao Y et al (2023) Task-based functional magnetic resonance imaging prediction of postsurgical cognitive outcomes in temporal lobe epilepsy: a systematic review, meta-analysis, and new data. Epilepsia 64:266–283. https://doi.org/10.1111/epi.17475. (PMID: 10.1111/epi.1747536522799) Forseth KJ, Kadipasaoglu CM, Conner CR et al (2018) A lexical semantic hub for heteromodal naming in middle fusiform gyrus. Brain 141:2112–2126. https://doi.org/10.1093/brain/awy120. (PMID: 10.1093/brain/awy120298602986365955) Mancini M, Vos SB, Vakharia VN et al (2019) Automated fiber tract reconstruction for surgery planning: extensive validation in language-related white matter tracts. NeuroImage Clin 23:101883. https://doi.org/10.1016/j.nicl.2019.101883. (PMID: 10.1016/j.nicl.2019.101883311633866545442) Binding LP, Dasgupta D, Giampiccolo D et al (2022) Structure and function of language networks in temporal lobe epilepsy. Epilepsia 63:1025–1040. https://doi.org/10.1111/epi.17204. (PMID: 10.1111/epi.17204351842919773900) Abdallah C, Brissart H, Colnat-Coulbois S et al (2021) Stereoelectroencephalographic language mapping of the basal temporal cortex predicts postoperative naming outcome. J Neurosurg. https://doi.org/10.3171/2020.8.JNS202431. (PMID: 10.3171/2020.8.JNS20243133636700) Giovagnoli AR, Parente A, Didato G et al (2016) The course of language functions after temporal lobe epilepsy surgery: a prospective study. Eur J Neurol 23:1713–1721. https://doi.org/10.1111/ene.13113. (PMID: 10.1111/ene.1311327529582) Helmstaedter C (2013) Cognitive outcomes of different surgical approaches in temporal lobe epilepsy. Epileptic Disord 15:221–239. https://doi.org/10.1684/epd.2013.0587. (PMID: 10.1684/epd.2013.058723899718) Schoenberg MR, Clifton WE, Sever RW, Vale FL (2018) Neuropsychology outcomes following trephine epilepsy surgery: the inferior temporal gyrus approach for amygdalohippocampectomy in medically refractory mesial temporal lobe epilepsy. Neurosurgery 82:833–841. https://doi.org/10.1093/neuros/nyx302. (PMID: 10.1093/neuros/nyx30228595352) Winston GP, Daga P, White MJ et al (2014) Preventing visual field deficits from neurosurgery. Neurology 83:604–611. https://doi.org/10.1212/WNL.0000000000000685. (PMID: 10.1212/WNL.0000000000000685250153634141993) Kapsalakis IZ, Kapsalaki EZ, Gotsis ED et al (2012) Preoperative evaluation with fMRI of patients with intracranial gliomas. Radiol Res Pract 2012:1–17. https://doi.org/10.1155/2012/727810. (PMID: 10.1155/2012/727810) Kim KK, Privitera MD, Szaflarski JP (2011) Lessons learned from a comparison of language localisation using fMRI and electrocortical mapping: case studies of neocortical epilepsy patients. Epileptic Disord 13:368–374. https://doi.org/10.1684/epd.2011.0473. (PMID: 10.1684/epd.2011.047322258040) You X, Zachery AN, Fanto EJ et al (2019) fMRI prediction of naming change after adult temporal lobe epilepsy surgery: activation matters. Epilepsia 60:527–538. https://doi.org/10.1111/epi.14656. (PMID: 10.1111/epi.14656307406666401285) Labudda K, Mertens M, Kalbhenn T et al (2017) Partial resection of presurgical fMRI activation is associated with a postsurgical loss of language function after frontal lobe epilepsy surgery. Neurocase 23:239–248. https://doi.org/10.1080/13554794.2017.1383445. (PMID: 10.1080/13554794.2017.138344528952404) |
| معلومات مُعتمدة: | P1904 Epilepsy Research UK; 14181 Brain Research UK |
| فهرسة مساهمة: | Keywords: Epilepsy surgery; Language fMRI; Language tracts; Naming outcome; Temporal lobe epilepsy; Tractography |
| تواريخ الأحداث: | Date Created: 20240407 Date Completed: 20240709 Latest Revision: 20240728 |
| رمز التحديث: | 20240728 |
| مُعرف محوري في PubMed: | PMC11233363 |
| DOI: | 10.1007/s00415-024-12315-2 |
| PMID: | 38583105 |
| قاعدة البيانات: | MEDLINE |
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| DOI: | 10.1007/s00415-024-12315-2 |