Abstract
While converging evidence suggests linguistic roles of white matter tracts, detailed associations between white matter alterations of dual pathways and language abilities remain unknown in aphasic patients. We aimed to verify language functions of dual-pathway tracts from specific domains and investigate the influence of moderators. PubMed, Web of Science, Embase, and CENTRAL were searched for studies published between January 1, 1985 and March 17, 2019. A meta-analysis of 46 studies including 1353 aphasic patients was performed by pooling correlation coefficients between linguistic domains and diffusion metrics of dual-pathway tracts. Among these tracts, the fractional anisotropy (FA) value of the left inferior fronto-occipital fasciculus predominated across most linguistic aspects, showing the strongest correlations with global severity, comprehension, naming and reading ability. The left uncinate fasciculus and inferior longitudinal fasciculus also showed significant FA − comprehension correlations. For syntactic processing, FA values of the left superior longitudinal fasciculus and arcuate fasciculus showed significant positive correlations. Meta-regression revealed no influence of etiology on FA − language correlations, while sex had a moderating effect on the FA − comprehension correlation of the arcuate fasciculus, and age influenced the FA − naming correlation in the superior longitudinal fasciculus. In conclusion, multifunctional characteristics of tracts were revealed in aphasic patients, including broad linguistic associations of the inferior fronto-occipital fasciculus, and repetition and syntactic involvement of the arcuate fasciculus. Language associations of the inferior longitudinal fasciculus and uncinate fasciculus were clarified regarding comprehension subdomains. The insignificant moderating effect of the etiology indicates damage of dual pathways is the common neural mechanism, while sex and age influence the correlation with comprehension and naming ability, respectively, in specific tracts.
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References
Agosta, F., Henry, R. G., Migliaccio, R., Neuhaus, J., Miller, B. L., Dronkers, N. F., et al. (2010). Language networks in semantic dementia. Brain, 133(1), 286–299. https://doi.org/10.1093/brain/awp233
Alexander, A. L., Lee, J. E., Lazar, M., & Field, A. S. (2007). Diffusion tensor imaging of the brain. Neurotherapeutics, 4(3), 316–329. https://doi.org/10.1016/j.nurt.2007.05.011
Assaf, Y., & Basser, P. J. (2005). Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. Neuroimage, 27(1), 48–58. https://doi.org/10.1016/j.neuroimage.2005.03.042
Azuar, C., Leger, A., Arbizu, C., Henry-Amar, F., Chomel-Guillaume, S., & Samson, Y. (2013). The Aphasia Rapid Test: an NIHSS-like aphasia test. Journal of Neurology, 260(8), 2110–2117. https://doi.org/10.1007/s00415-013-6943-x
Basser, P. J., & Jones, D. K. (2002). Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review. NMR in Biomedicine, 15(7–8), 456–467. https://doi.org/10.1002/nbm.783
Bonilha, L., Hillis, A. E., Hickok, G., den Ouden, D. B., Rorden, C., & Fridriksson, J. (2017). Temporal lobe networks supporting the comprehension of spoken words. Brain, 140, 2370–2380. https://doi.org/10.1093/brain/awx169
Catani, M., Dell’acqua, F., Vergani, F., Malik, F., Hodge, H., Roy, P., et al. (2012). Short frontal lobe connections of the human brain. Cortex, 48(2), 273–291. https://doi.org/10.1016/j.cortex.2011.12.001
Catani, M., Howard, R. J., Pajevic, S., & Jones, D. K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage, 17(1), 77–94. https://doi.org/10.1006/nimg.2002.1136
Catani, M., Jones, D. K., Donato, R., & Ffytche, D. H. (2003). Occipito-temporal connections in the human brain. Brain, 126(Pt 9), 2093–2107. https://doi.org/10.1093/brain/awg203
Catani, M., Jones, D. K., & ffytche, D. H. . (2005). Perisylvian language networks of the human brain. Annals of Neurology, 57(1), 8–16. https://doi.org/10.1002/ana.20319
Catani, M., Mesulam, M. M., Jakobsen, E., Malik, F., Martersteck, A., Wieneke, C., et al. (2013). A novel frontal pathway underlies verbal fluency in primary progressive aphasia. Brain, 136(Pt 8), 2619–2628. https://doi.org/10.1093/brain/awt163
Chang, E. F., Raygor, K. P., & Berger, M. S. (2015). Contemporary model of language organization: an overview for neurosurgeons. Journal of Neurosurgery, 122(2), 250–261. https://doi.org/10.3171/2014.10.JNS132647
Cloutman, L. L. (2013). Interaction between dorsal and ventral processing streams: where, when and how? Brain and Language, 127(2), 251–263. https://doi.org/10.1016/j.bandl.2012.08.003
Crutch, S. J., & Warrington, E. K. (2003). Spatial coding of semantic information: knowledge of country and city names depends on their geographical proximity. Brain, 126(Pt 8), 1821–1829. https://doi.org/10.1093/brain/awg187
Crutch, S. J., & Warrington, E. K. (2004). The semantic organisation of proper nouns: the case of people and brand names. Neuropsychologia, 42(5), 584–596. https://doi.org/10.1016/j.neuropsychologia.2003.10.009
Dick, A. S., Bernal, B., & Tremblay, P. (2014). The language connectome: new pathways, new concepts. Neuroscientist, 20(5), 453–467. https://doi.org/10.1177/1073858413513502
Dick, A. S., & Tremblay, P. (2012). Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain, 135(Pt 12), 3529–3550. https://doi.org/10.1093/brain/aws222
Dronkers, N. F., Plaisant, O., Iba-Zizen, M. T., & Cabanis, E. A. (2007). Paul Broca’s historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. Brain, 130(Pt 5), 1432–1441. https://doi.org/10.1093/brain/awm042
Duffau, H., Herbet, G., & Moritz-Gasser, S. (2013). Toward a pluri-component, multimodal, and dynamic organization of the ventral semantic stream in humans: lessons from stimulation mapping in awake patients. Frontiers in Systems Neuroscience, 7, 44. https://doi.org/10.3389/fnsys.2013.00044
Elbourn, E., Kenny, B., Power, E., Honan, C., McDonald, S., Tate, R., et al. (2019). Discourse recovery after severe traumatic brain injury: exploring the first year. Brain Injury, 33(2), 143–159. https://doi.org/10.1080/02699052.2018.1539246
Forkel, S. J., De Schotten, M. T., Dell’Acqua, F., Kalra, L., Murphy, D. G. M., Williams, S. C. R., et al. (2014). Anatomical predictors of aphasia recovery: A tractography study of bilateral perisylvian language networks. Brain, 137(7), 2027–2039. https://doi.org/10.1093/brain/awu113
Forkel, S. J., Rogalski, E., Drossinos Sancho, N., D’Anna, L., Luque Laguna, P., Sridhar, J., et al. (2020). Anatomical evidence of an indirect pathway for word repetition. Neurology, 94(6), e594–e606. https://doi.org/10.1212/WNL.0000000000008746
Forkel, S. J., Thiebaut de Schotten, M., Kawadler, J. M., Dell’Acqua, F., Danek, A., & Catani, M. (2014). The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography. Cortex, 56, 73–84. https://doi.org/10.1016/j.cortex.2012.09.005
Friederici, A. D. (2012). The cortical language circuit: from auditory perception to sentence comprehension. Trendsin Cognitive Sciences, 16(5), 262–268. https://doi.org/10.1016/j.tics.2012.04.001
Friederici, A. D., Bahlmann, J., Heim, S., Schubotz, R. I., & Anwander, A. (2006). The brain differentiates human and non-human grammars: functional localization and structural connectivity. Proceedings of the National Academy of Sciences of the United States of America, 103(7), 2458–2463. https://doi.org/10.1073/pnas.0509389103
Friederici, A. D., & Gierhan, S. M. (2013). The language network. Current Opinion in Neurobiology, 23(2), 250–254. https://doi.org/10.1016/j.conb.2012.10.002
Gao, S. R. (2006). Aphasia (2nd ed.). Beijing, China: Peking University Medical Press.
Gierhan, S. M. E. (2013). Connections for auditory language in the human brain. Brain and Language, 127(2), 205–221. https://doi.org/10.1016/j.bandl.2012.11.002
Gil-Robles, S., Carvallo, A., Jimenez Mdel, M., Gomez Caicoya, A., Martinez, R., Ruiz-Ocana, C., et al. (2013). Double dissociation between visual recognition and picture naming: a study of the visual language connectivity using tractography and brain stimulation. Neurosurgery, 72(4), 678–686. https://doi.org/10.1227/NEU.0b013e318282a361
Glasser, M. F., & Rilling, J. K. (2008). DTI tractography of the human brain’s language pathways. Cerebral Cortex, 18(11), 2471–2482. https://doi.org/10.1093/cercor/bhn011
Gorno-Tempini, M. L., Price, C. J., Josephs, O., Vandenberghe, R., Cappa, S. F., Kapur, N., et al. (1998). The neural systems sustaining face and proper-name processing. Brain, 121(Pt 11), 2103–2118. https://doi.org/10.1093/brain/121.11.2103
Griffiths, J. D., Marslen-Wilson, W. D., Stamatakis, E. A., & Tyler, L. K. (2013). Functional organization of the neural language system: dorsal and ventral pathways are critical for syntax. Cerebral Cortex, 23(1), 139–147. https://doi.org/10.1093/cercor/bhr386
Han, Z., Ma, Y., Gong, G., He, Y., Caramazza, A., & Bi, Y. (2013). White matter structural connectivity underlying semantic processing: evidence from brain damaged patients. Brain, 136, 2952–2965. https://doi.org/10.1093/brain/awt205
Han, Z., Ma, Y., Gong, G., Huang, R., Song, L., & Bi, Y. (2016). White matter pathway supporting phonological encoding in speech production: a multi-modal imaging study of brain damage patients. Brain Structure and Function, 221(1), 577–589. https://doi.org/10.1007/s00429-014-0926-2
Hickok, G., & Poeppel, D. (2007). The cortical organization of speech processing. Nature Reviews Neuroscience, 8(5), 393–402. https://doi.org/10.1038/nrn2113
Hulkower, M. B., Poliak, D. B., Rosenbaum, S. B., Zimmerman, M. E., & Lipton, M. L. (2013). A decade of DTI in traumatic brain injury: 10 years and 100 articles later. AJNR: American Journal of Neuroradiology, 34(11), 2064–2074. https://doi.org/10.3174/ajnr.A3395
Ivanova, M. V., Isaev, D. Y., Dragoy, O. V., Akinina, Y. S., Petrushevskiy, A. G., Fedina, O. N., et al. (2016). Diffusion-tensor imaging of major white matter tracts and their role in language processing in aphasia. Cortex, 85, 165–181. https://doi.org/10.1016/j.cortex.2016.04.019
Jang, S. H., Cho, I. T., & Lim, J. W. (2017). Recovery of aphasia and change of injured arcuate fasciculus in the dominant hemisphere in stroke patients. NeuroRehabilitation, 41(4), 759–764. https://doi.org/10.3233/nre-172167
Jensen, J. H., Helpern, J. A., Ramani, A., Lu, H., & Kaczynski, K. (2005). Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magnetic Resonance in Medicine, 53(6), 1432–1440. https://doi.org/10.1002/mrm.20508
Jung, M., Mody, M., Fujioka, T., Kimura, Y., Okazawa, H., & Kosaka, H. (2019). Sex Differences in White Matter Pathways Related to Language Ability. Frontiers in Neuroscience, 13, 898. https://doi.org/10.3389/fnins.2019.00898
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test (2nd ed.). Philadelphia: Lea & Febiger.
Kertesz, A. (2007). Western aphasia battery revised (Examiner’s manual, Vol. 1). San Antonio, TX: Harcourt Assessment, Inc.
Kim, S. H., & Jang, S. H. (2013). Prediction of aphasia outcome using diffusion tensor tractography for arcuate fasciculus in stroke. AJNR: American Journal of Neuroradiology, 34(4), 785–790. https://doi.org/10.3174/ajnr.A3259
Li, D., Bao, S., & Ma, L. (2004). The study on the relationship between various b-values and the anisotropy index in diffusion tensor imaging. Chinese Journal of Radiology, 38(12), 1238–1242.
Makris, N., Kennedy, D. N., McInerney, S., Sorensen, A. G., Wang, R., Caviness, V. S., Jr., et al. (2005). Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo. DT-MRI study. Cerebral Cortex, 15(6), 854–869. https://doi.org/10.1093/cercor/bhh186
Makris, N., Papadimitriou, G. M., Kaiser, J. R., Sorg, S., Kennedy, D. N., & Pandya, D. N. (2009). Delineation of the middle longitudinal fascicle in humans: a quantitative, in vivo. DT-MRI study. Cerebral Cortex, 19(4), 777–785. https://doi.org/10.1093/cercor/bhn124
Mandonnet, E., Nouet, A., Gatignol, P., Capelle, L., & Duffau, H. (2007). Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain, 130(Pt 3), 623–629. https://doi.org/10.1093/brain/awl361
Martino, J., Brogna, C., Robles, S. G., Vergani, F., & Duffau, H. (2010). Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex, 46(5), 691–699. https://doi.org/10.1016/j.cortex.2009.07.015
McKinnon, E. T., Fridriksson, J., Glenn, G. R., Jensen, J. H., Helpern, J. A., Basilakos, A., et al. (2017). Structural plasticity of the ventral stream and aphasia recovery. Annals of Neurology, 82(1), 147–151. https://doi.org/10.1002/ana.24983
Melhem, E. R., Itoh, R., Jones, L., & Barker, P. B. (2000). Diffusion tensor MR imaging of the brain: Effect of diffusion weighting on trace and anisotropy measurements. American Journal of Neuroradiology, 21(10), 1813–1820.
Menjot de Champfleur, N., Lima Maldonado, I., Moritz-Gasser, S., Machi, P., Le Bars, E., Bonafe, A., et al. (2013). Middle longitudinal fasciculus delineation within language pathways: a diffusion tensor imaging study in human. European Journal of Radiology, 82(1), 151–157. https://doi.org/10.1016/j.ejrad.2012.05.034
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Group, P. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ, 339, b2535. https://doi.org/10.1136/bmj.b2535
Papagno, C., Miracapillo, C., Casarotti, A., Romero Lauro, L. J., Castellano, A., Falini, A., et al. (2011). What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain, 134(Pt 2), 405–414. https://doi.org/10.1093/brain/awq283
Patel, A. D. (2003). Language, music, syntax and the brain. Nature Neuroscience, 6(7), 674–681. https://doi.org/10.1038/nn1082
Raffelt, D. A., Tournier, J. D., Smith, R. E., Vaughan, D. N., Jackson, G., Ridgway, G. R., et al. (2017). Investigating white matter fibre density and morphology using fixel-based analysis. Neuroimage, 144(Pt A), 58–73. https://doi.org/10.1016/j.neuroimage.2016.09.029
Rosso, C., Vargas, P., Valabregue, R., Arbizu, C., Henry-Amar, F., Leger, A., et al. (2015). Aphasia severity in chronic stroke patients: a combined disconnection in the dorsal and ventral language pathways. Neurorehabilitation and Neural Repair, 29(3), 287–295. https://doi.org/10.1177/1545968314543926
Sarubbo, S., De Benedictis, A., Maldonado, I. L., Basso, G., & Duffau, H. (2013). Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Structure and Function, 218(1), 21–37. https://doi.org/10.1007/s00429-011-0372-3
Sathian, K., & Crosson, B. (2015). Structure-function correlations in stroke. Neuron, 85(5), 887–889. https://doi.org/10.1016/j.neuron.2015.02.031
Saur, D., Kreher, B. W., Schnell, S., Kummerer, D., Kellmeyer, P., Vry, M. S., et al. (2008). Ventral and dorsal pathways for language. Proceedings of the National Academy of Sciences of the United States of America, 105(46), 18035–18040. https://doi.org/10.1073/pnas.0805234105
Sierpowska, J., Leon-Cabrera, P., Camins, A., Juncadella, M., Gabarros, A., & Rodriguez-Fornells, A. (2020). The black box of global aphasia: Neuroanatomical underpinnings of remission from acute global aphasia with preserved inner language function. Cortex, 130, 340–350. https://doi.org/10.1016/j.cortex.2020.06.009
Thiebaut de Schotten, M., Dell’Acqua, F., Forkel, S. J., Simmons, A., Vergani, F., Murphy, D. G., et al. (2011). A lateralized brain network for visuospatial attention. Nature Neuroscience, 14(10), 1245–1246. https://doi.org/10.1038/nn.2905
Tremblay, P., & Dick, A. S. (2016). Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain and Language, 162, 60–71. https://doi.org/10.1016/j.bandl.2016.08.004
Troutman, S. B. W., & Diaz, M. T. (2019). White matter disconnection is related to age-related phonological deficits. Brain Imaging and Behavior. https://doi.org/10.1007/s11682-019-00086-8
Ulugut Erkoyun, H., Groot, C., Heilbron, R., Nelissen, A., van Rossum, J., Jutten, R., et al. (2020). A clinical-radiological framework of the right temporal variant of frontotemporal dementia. Brain. https://doi.org/10.1093/brain/awaa225
Wilson, S. M., Galantucci, S., Tartaglia, M. C., Rising, K., Patterson, D. K., Henry, M. L., et al. (2011). Syntactic processing depends on dorsal language tracts. Neuron, 72(2), 397–403. https://doi.org/10.1016/j.neuron.2011.09.014
Wu, Y., Sun, D., Wang, Y., & Wang, Y. (2016). Subcomponents and Connectivity of the Inferior Fronto-Occipital Fasciculus Revealed by Diffusion Spectrum Imaging Fiber Tracking. Frontiers in Neuroanatomy, 10, 88. https://doi.org/10.3389/fnana.2016.00088
Zhang, H., Schneider, T., Wheeler-Kingshott, C. A., & Alexander, D. C. (2012). NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage, 61(4), 1000–1016. https://doi.org/10.1016/j.neuroimage.2012.03.072
Zhang, J., Wei, X., Xie, S., Zhou, Z., Shang, D., Ji, R., et al. (2018). Multifunctional Roles of the Ventral Stream in Language Models: Advanced Segmental Quantification in Post-Stroke Aphasic Patients. Frontiers in Neurology, 9, 89. https://doi.org/10.3389/fneur.2018.00089
Zhang, W., Liang, B., Ye, R., Liang, B., Ye, R., & Huang, H. (2004). Effect of Different Diffusion Weighting on ADC and FA Measurements of Normal Brain. Chinese Computed Medical Imaging, 10(2), 81–85.
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This study was supported by the grants from National Natural Science Foundation of P. R. China (No. 81902278), Zhejiang Provincial Natural Science Foundation (No. LGF20H170011), and the Science and Technology Planning Project of Zhejiang Province, P. R. China (2017C03011).
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Benyan Luo designed the study, and Jie Zhang and Shuchang Zhong were responsible for literature search. Yamei Yu and Min Wu extracted data and assessed the quality. Li Zhang, Yanmei Yu and Xufei Tan checked the data and solved disagreements. Jie Zhang, Yanfei Wu and Peng Sun contributed to statistical analysis. Jie Zhang drafted the manuscript; Ruidong Cheng plotted figures, and improved the interpretation of data; Liang Zhou and Wei Zhang contributed to the manuscript revision and responded to the reviewers’ comments with helpful ideas; and Juebao Li and Xiangming Ye supervised and revised it.
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Zhang, J., Zhong, S., Zhou, L. et al. Correlations between Dual-Pathway White Matter Alterations and Language Impairment in Patients with Aphasia: A Systematic Review and Meta-analysis. Neuropsychol Rev 31, 402–418 (2021). https://doi.org/10.1007/s11065-021-09482-8
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DOI: https://doi.org/10.1007/s11065-021-09482-8