Altered brain structures in the dorsal and ventral language pathways in individuals with and without developmental language disorder (DLD)

Abstract

Developmental Language Disorder (DLD) is a neurodevelopmental disorder characterized by difficulty learning and using language, and this difficulty cannot be attributed to other developmental conditions. The aim of the current study was to examine structural differences in dorsal and ventral language pathways between adolescents and young adults with and without DLD (age range: 14–27 years) using anatomical magnetic resonance imaging (MRI) and diffusion tensor imaging (DTI). Results showed age-related structural brain differences in both dorsal and ventral pathways in individuals with DLD. These findings provide evidence for neuroanatomical correlates of persistent language deficits in adolescents/young adults with DLD, and further suggest that this brain-language relationship in DLD is better characterized by taking account the dynamic course of the disorder along development.

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Notes

  1. 1.

    The TTG is part of both dorsal and ventral pathways. For the purpose of simplicity, we categorize it as one of the ROIs in the dorsal pathway. It is because the primary function of the TTG is speech processing (e.g., processing spectral properties of sounds), which is a major function of the dorsal pathway.

  2. 2.

    Absolute volumes were provided in order that the current findings could be compared to those that were not corrected for ICV. Our statistical analyses were limited to the relative values.

References

  1. Alexander, A. L., Lee, J. E., Lazar, M., & Field, A. S. (2007). Diffusion tensor imaging of the brain. Neurotherapeutics, 4, 316–329.

    PubMed  PubMed Central  Google Scholar 

  2. Anthony, J. L., Davis, C., Williams, J. M., & Anthony, T. I. (2014). Preschoolers’ oral language ability: a multilevel examination of dimensionality. Learning and Individual Differences, 35, 56–61.

    Google Scholar 

  3. Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences, 8(4), 170–177.

    PubMed  Google Scholar 

  4. Asato, M. R., Terwilliger, R., Woo, J., & Luna, B. (2010). White matter development in adolescence: a DTI study. Cerebral Cortex, 20(9), 2122–2131.

    CAS  PubMed  Google Scholar 

  5. Badcock, N. A., Bishop, D. V. M., Hardiman, M. J., Barry, J. G., & Watkins, K. E. (2012). Co-localisation of abnormal brain structure and function in specific language impairment. Brain and Language, 120(3), 310–320.

    PubMed  PubMed Central  Google Scholar 

  6. Bailey, P., & Snowling, M. (2002). Auditory processing and the development of language and literacy. British Medical Bulletin, 63(1), 135–146.

    PubMed  Google Scholar 

  7. Bajada, C. J., Lambon Ralph, M. A., & Cloutman, L. L. (2015). Transport for language south of the Sylvian fissure: the routes and history of the main tracts and stations in the ventral language network. Cortex, 69, 141–151.

    PubMed  Google Scholar 

  8. Barnea-Goraly, N., Menon, V., Eckert, M., Tamm, L., Bammer, R., Karchemskiy, A., et al. (2005). White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cerebral Cortex, 15(12), 1848–1854.

    PubMed  Google Scholar 

  9. Benasich, A. A., Thomas, J. J., Choudhury, N., & Leppanen, P. H. T. (2002). The importance of rapid auditory processing abilities to early language development: evidence from converging methodologies. Developmental Psychobiology, 40(3), 278–292.

    PubMed  PubMed Central  Google Scholar 

  10. Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B, 57(1), 289–300.

    Google Scholar 

  11. Bishop, D. V. M. (2000). How does the brain learn language? Insights from the study of children with and without language impairment. Developmental Medicine and Child Neurology, 42, 133–142.

    CAS  PubMed  Google Scholar 

  12. Bishop, D. V. M. (2013). Cerebral asymmetry and language development: cause, correlate or consequence? Science, 340(6138), 1230531.

    PubMed  PubMed Central  Google Scholar 

  13. Bishop, D. V. M., & McArthur, G. M. (2005). Individual differences in auditory processing in specific language impairment: a follow-up study using event-related potentials and behavioral thresholds. Cortex, 41(3), 327–341.

    PubMed  PubMed Central  Google Scholar 

  14. Bishop, D. V. M., Carlyon, R. P., Deeks, J. M., & Bishop, S. J. (1999). Auditory temporal processing impairment: neither necessary nor sufficient for causing language impairment in children. Journal of Speech, Language, and Hearing Research, 42(6), 1295–1310.

    CAS  PubMed  Google Scholar 

  15. Bornstein, M. H., Hahn, C. S., Putnick, D. L., & Suwalsky, J. T. D. (2014). Stability of core language skill from early childhood to adolescence: a latent variable approach. Child Development, 85(4), 1346–1356.

    PubMed  PubMed Central  Google Scholar 

  16. Brauer, J., Anwander, A., & Friederici, A. D. (2011). Neuroanatomical prerequisites for language functions in the maturing brain. Cerebral Cortex, 21, 459–466.

    PubMed  Google Scholar 

  17. Brauer, J., Anwander, A., Perani, D., & Friederici, A. D. (2013). Dorsal and ventral pathways in language development. Brain and Language, 127(2), 289–295.

    PubMed  Google Scholar 

  18. Broce, I., Bernal, B., Altman, N., Tremblay, P., & Dick, A. S. (2015). Fiber tracking of the frontal aslant tract and subcomponents of the arcuate fasciculus in 5–8-year-olds: relation to speech and language function. Brain and Language, 149, 66–76.

    PubMed  Google Scholar 

  19. Catani, M., Jones, D. K., & Ffytche, D. H. (2005). Perisylvian language networks of the human brain. Annual Neurology, 57(1), 8–16.

    Google Scholar 

  20. Cheng, P., Magnotta, V. A., Wu, D., Nopoulos, P., Moser, D. J., Paulsen, J., et al. (2006). Evaluation of the GTRACT diffusion tensor tractography algorithm: a validation and reliability study. NeuroImage, 31(3), 1075–1085.

    PubMed  Google Scholar 

  21. Clark, M. M., & Plante, E. (1998). Morphology of the inferior frontal gyrus in developmentally language-disordered adults. Brain and Language, 61(2), 288–303.

    CAS  PubMed  Google Scholar 

  22. Cloutman, L. L. (2013). Interaction between dorsal and ventral processing streams: where, when, and how? Brain and Language, 127(2), 251–263.

    PubMed  Google Scholar 

  23. Coady, J. A., Kluender, K. R., & Evans, J. L. (2005). Categorical perception of speech by children with specific language impairments. Journal of Speech, Language, and Hearing Research, 48(4), 944–959.

    PubMed  PubMed Central  Google Scholar 

  24. Cohen, M., Campbell, R., & Yaghmai, F. (1989). Neuropathological abnormalities in developmental dysphasia. Annals of Neurology, 25(6), 567–570.

    CAS  PubMed  Google Scholar 

  25. Corriveau, K., Pasquini, E., & Goswami, U. (2007). Basic auditory processing skills and specific language impairment: a new look at an old hypothesis. Journal of Speech, Language, and Hearing Research, 50, 647–666.

    PubMed  Google Scholar 

  26. Cristia, A., Seidl, A., Junge, C., Soderstrom, M., & Hagoort, P. (2014). Predicting individual variation in language from infant speech perception measures. Child Development, 85(4), 1330–1345.

    PubMed  Google Scholar 

  27. Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194.

    CAS  PubMed  Google Scholar 

  28. De Fossé, L., Hodge, S. M., Makris, N., Kennedy, D. N., Caviness, V. S. Jr., McGrath, L., … Harris, G. J. (2004). Language-association cortex asymmetry in autism and specific language impairment. Annals of Neurology, 56(6), 757–766.

  29. De Guibert, C., Maumet, C., Jannin, P., Ferre, J.-C., Treguier, C., Barillot, C., et al. (2011). Abnormal functional lateralization and activity of language brain areas in typical specific language impairment. Brain, 134(10), 3044–3058.

    PubMed  PubMed Central  Google Scholar 

  30. De Renzi, E., & Faglioni, P. (1978). Normative data and screening power of a shortened version of the Token Test. Cortex, 14, 41–49.

    PubMed  Google Scholar 

  31. Dick, A. S., Bernal, B., & Tremblay, P. (2014). The language connectome: new pathways, new concepts. Neuroscientist, 20(5), 453–467.

    PubMed  Google Scholar 

  32. Dollaghan, C. A. (2011). Taxometric analyses of specific language impairment in 6-year-old children. Journal of Speech, Language, and Hearing Research, 54, 1361–1371.

    PubMed  Google Scholar 

  33. 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), 1–4.

    Google Scholar 

  34. Dunn, L. M., & Dunn, D. M. (2007). Peabody picture vocabulary test-fourth edition (PPVT-4). MN: Pearson.

    Google Scholar 

  35. Evans, J. (2001). An emergent account of language impairments in children with SLI: implications for assessment and intervention. Journal of Communication Disorders, 34(1–2), 39–54.

    CAS  PubMed  Google Scholar 

  36. Fischl, B., Sereno, M. I., Tootell, R. B. H., & Dale, A. M. (1999). High-resolution inter-subject averaging and a coordinate system for the cortical surface. Human Brain Mapping, 8, 272–284.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Fischl, B., Liu, A., & Dale, A. M. (2001). Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transactions on Medical Image, 20(1), 70–80.

    CAS  Google Scholar 

  38. Friederici, A. D. (2009). Pathways to language: Fiber tracts in the human brain. Trends in Cognitive Sciences, 13(4), 175–181.

    PubMed  Google Scholar 

  39. Friederici, A. D., & Gierhan, S. (2013). The language network. Current Opinion in Neurobiology, 23, 250–254.

    CAS  Google Scholar 

  40. Gauger, L. M., Lombardino, I. J., & Leonard, C. M. (1997). Brain morphology in children with specific language impairment. Journal of Speech, Language, and Hearing Research, 40, 1272–1284.

    CAS  PubMed  Google Scholar 

  41. Glasser, M. F., & Rilling, J. K. (2008). DTI Tractography of the human brain’s language pathways. Cerebral Cortex, 18(11), 2471–2482.

    PubMed  Google Scholar 

  42. Hammill, D. D., Brown, V. L., Larsen, S. C., & Wiederholt, J. L. (2007). Test of adolescent and adult language, fourth edition (TOAL-4). Austin: Pro-Ed.

    Google Scholar 

  43. Harris, G., Andreasen, N. C., Cizadlo, T., Bailey, J. M., Bockholt, H. J., Magnotta, V. A., & Arndt, S. (1999). Improving tissue classification in MRI: a three-dimensional multispectral discriminant analysis method with automated training class selection. Journal of Computer Assisted Tomography, 23(1), 144–154.

    CAS  PubMed  Google Scholar 

  44. Helzer, J. R., Champlin, C. A., & Gillam, R. B. (1996). Auditory temporal resolution in specifically language-impaired and age-matched children. Perceptual and Motor Skills, 83(3), 1171–1181.

    CAS  PubMed  Google Scholar 

  45. Henry, L. A., Messer, D. J., & Nash, G. (2012). Executive functioning in children with specific language impairment. Journal of Child Psychology and Psychiatry, 53(1), 37–45.

    PubMed  Google Scholar 

  46. Hepper, P. (2015). Behavior during the prenatal period: adaptive for development and survival. Child Development Perspectives, 9(1), 38–43.

    Google Scholar 

  47. Herbert, M. R., Ziegler, D. A., Makris, N., Bakardjiev, A., Hodgson, J., Adrien, K. T., … Caviness Jr., V. S. (2003). Larger brain and white matter volumes in children with developmental language disorder. Developmental Science, 6(4), F11-F22.

  48. Herbert, M. R., Ziegler, D. A., Makris, N., Filipek, P. A., Kemper, T. L., Normandin, J. J., … Caviness, V. S. (2004). Localization of white matter volume increase in autism and developmental language disorder. Annals of Neurology, 55(4), 530–540.

  49. Herbert, M.R., Ziegler, D. A., Deutsch, C. K., O’Brien, L. M., Kennedy, D. N., Filipek, P. A., … Caviness, V. S. (2005). Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis. Brain, 128, 213–226.

  50. Hickok, G., & Poeppel, D. (2004). Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition, 92(1–2), 67–99.

    PubMed  Google Scholar 

  51. Hofer, S., & Frahm, J. (2006). Topography of the human corpus callosum revisited--comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. NeuroImage, 32(3), 989–994.

    PubMed  Google Scholar 

  52. Hua, K., Zhang, J., Wakana, S., Jiang, H., Li, X., Reich, D. S., … Mori, S. (2008). Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. NeuroImage, 39(1), 336–347.

  53. Hugdahl, K., Gundersen, H., Brekke, C., Thomsen, T., Rimol, L. M., Ersland, L., & Niemi, J. (2004). FMRI brain activation in a Finnish family with specific language impairment compared with a normal control group. Journal of Speech, Language, and Hearing Research, 47, 162–172.

    PubMed  Google Scholar 

  54. Huppi, P. S., & Dubois, J. (2006). Diffusion tensor imaging of brain development. Seminars in Fetal and Neonatal Medicine, 11(6), 489–497.

    PubMed  Google Scholar 

  55. Jancke, L., Siegenthaler, T., Preis, S., & Steinmetz, H. (2007). Decreased white-matter density in a left-sided fronto-temporal network in children with developmental language disorder: evidence for anatomical anomalies in a motor-language network. Brain and Language, 102, 91–98.

    CAS  PubMed  Google Scholar 

  56. Jernigan, T. L., Hesselink, J. R., Sowell, E., & Tallal, P. A. (1991). Cerebral structure on magnetic resonance imaging in language- and learning-impaired children. Archives of Neurology, 48, 539–545.

    CAS  PubMed  Google Scholar 

  57. Kamali, A., Flanders, A. E., Brody, J., Hunter, J. V., & Hasan, K. M. (2014). Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Structure and Function, 219(1), 269–281.

    PubMed  Google Scholar 

  58. Karmiloff-Smith, A. (1998). Development itself is the key to understanding developmental disorders. Trends in Cognitive Sciences, 2(10), 389–398.

    CAS  PubMed  Google Scholar 

  59. Kochunov, P., Williamson, D. E., Lancaster, J., Fox, P., Cornell, J., Blangero, J., & Glahn, D. C. (2012). Fractional anisotropy of water diffusion in cerebral white matter across the lifespan. Neurobiology of Aging, 33(1), 9–20.

    CAS  PubMed  Google Scholar 

  60. Krishnan, S., Watkins, K. E., & Bishop, D. V. M. (2016). Neurobiological basis of language learning difficulties. Trends in Cognitive Sciences, 20(9), 701–714.

    PubMed  PubMed Central  Google Scholar 

  61. Kurth, F., Luders, E., Pigdon, L., Conti-Ramsden, G., Reilly, S., & Morgan, A. T. (2018). Altered gray matter volumes in language-associated regions in children with developmental language disorder and speech sound disorder. Developmental Psychobiology, 60(7), 814–824.

    PubMed  Google Scholar 

  62. Kwok, E. Y. L., Joanisse, M. F., Archibald, L. M. D., & Cardy, J. O. (2018). Immature auditory evoked potentials in children with moderate-severe developmental language disorder. Journal of Speech, Language, and Hearing Research, 61, 1718–1730.

    PubMed  Google Scholar 

  63. Lambon Ralph, M. A., Pobric, G., & Jefferies, E. (2009). Conceptual knowledge is underpinned by the temporal pole bilaterally: convergent evidence from rTMS. Cerebral Cortex, 19(4), 832–838.

    PubMed  Google Scholar 

  64. Language and Reading Research Consortium. (2015). The dimensionality of language asbility in young children. Child Development, 86(6), 1948–1965.

    Google Scholar 

  65. Lebel, C., Gee, M., Camicioli, R., Wieler, M., Martin, W., & Beaulieu, C. (2012). Diffusion tensor imaging of white matter tract evolution over the lifespan. NeuroImage, 60(1), 340–352.

    CAS  PubMed  Google Scholar 

  66. Lee, J. C., Nopoulos, P. C., & Tomblin, J. B. (2013). Abnormal subcortical components of the corticostriatal system in young adults with DLI: a combined structural MRI and DTI study. Neuropsychologia, 51(11), 2154–2161.

    PubMed  Google Scholar 

  67. Leonard, L. B. (1998). Children with specific language impairment. Cambridge: MIT Press.

    Google Scholar 

  68. Leonard, L. B. (2014). Children with specific language impairment and their contribution to the study of language development. Journal of Child Language, 41(S1), 38–47.

    PubMed  PubMed Central  Google Scholar 

  69. Leonard, C. M., Lombardino, L. J., Walsh, K., Eckert, M. A., Mockler, J. L., Rowe, L. A., et al. (2002). Anatomical risk factors that distinguish dyslexia from SLI predict reading skill in normal children. Journal of Communication Disorders, 35, 501–531.

    PubMed  Google Scholar 

  70. Leroy, F., Glasel, H., Dubois, J., Hertz-Pannier, L., Thirlon, B., Mangin, J., & Dehaene-Lambetz, G. (2011). Early maturation of the linguistic dorsal pathway in human infants. Journal of Neuroscience, 31(4), 1500–1506.

    CAS  PubMed  Google Scholar 

  71. Lieberman, P. (2002). On the nature and evolution of the neural bases of human language. Yearbook of Physical Anthropology, 45, 36–62.

    Google Scholar 

  72. Liégeois, F. J., Turner, S. J., Mayes, A., Bonthrone, A. F., Boys, A., Smith, L., et al. (2019). Dorsal language stream anomalies in an inherited speech disorder. Brain, 142(4), 966–977.

    PubMed  Google Scholar 

  73. Liu, Z., Wang, Y., Gerig, G., Gouttard, S., Tao, R., Fletcher, T., & Styner, M. (2010). Quality control of diffusion weighted images. Proceedings of SPIE, 11, 7628.

    Google Scholar 

  74. Magnotta, V. A., Heckel, D., Andreasen, N. C., Cizadlo, T., Corson, P. W., Ehrhardt, J. C., et al. (1999). Measurement of brain structures with artificial neural networks: two- and three-dimensional applications. Radiology, 211(3), 781–790.

    CAS  PubMed  Google Scholar 

  75. Magnotta, V. A., Harris, G., Andreasen, N. C., O’Leary, D. S., Yuh, W. T., & Heckel, D. (2002). Structural MR image processing using the BRAINS2 toolbox. Computerized Medical Imaging and Graphics, 26(4), 251–264.

    PubMed  Google Scholar 

  76. Mareschal, D., Johnson, M. H., Sirios, S., Spratling, M., Thomas, M. S. C., & Westermann, G. (2007). Neuroconstructivism. Vol. I. Heow the brain constructs cognition. Oxford, England: Oxford University Press.

  77. Markanday, S., Brennan, S. L., Gould, H., & Pasco, J. A. (2013). Sex-differences in reasons for non-participation at recruitment: Geelong Osteoporosis Study. BMC Research Notes, 6(104), 1–7.

    Google Scholar 

  78. Martino, J., De Witt Hamer, P. C., Berger, M. S., Lawton, M. T., Arnold, C. M., de Lucas, E. M., & Duffau, H. (2013). Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Structure and Function, 218(1), 105–121.

    PubMed  Google Scholar 

  79. McDonald, C. R., Ahmadi, M. E., Hagler, D. J., Tecoma, E. S., Iragui, V. J., Gharapetian, L., … Halgren, E. (2008). Diffusion tensor imaging correlates of memory and language impairments in temporal lobe epilepsy. Neurology, 71, 1869–1876.

  80. Merzenich, M. M., Jenkins, W. M., Johnston, P., Schreiner, C., Miller, S. L., & Tallal, P. (1996). Temporal processing deficits of language-learning impaired children ameliorated by training. Science, 271(5245), 77–81.

    CAS  PubMed  Google Scholar 

  81. Mesulam, M. (1990). Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Annals of Neurology, 28(5), 597–613.

    CAS  PubMed  Google Scholar 

  82. Moon, C., Lagercrantz, H., & Huhl, P. K. (2013). Language experienced in utero affects vowel perception after birth: a two-country study. Acta Paediatrica, 102(2), 156–160.

    PubMed  Google Scholar 

  83. Morgan, A. T., Su, M., Reilly, S., Conti-Ramsden, G., Connelly, A., & Liégeois, F. J. (2018). A brain marker for developmental speech disorders. The Journal of Pediatrics, 198, 234–239.

    PubMed  Google Scholar 

  84. Morice, R., & McNicol, D. (1985). The comprehension and production of complex syntax in schizophrenia. Cortex, 21, 567–580.

    CAS  PubMed  Google Scholar 

  85. Morosan, P., Rademacher, J., Schleicher, A., Amunts, K., Schormann, T., & Zilles, K. (2001). Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. NeuroImage, 13(4), 685–701.

    Google Scholar 

  86. Nation, K. (2014). Lexical learning and lexical processing in children with developmental language impairments. Philosophical Transactions of the Royal Society B, 369, 20120387.

    Google Scholar 

  87. Norbury, C. F., Tomblin, J. B., & Bishop, D. V. (Eds.). (2008). Understanding developmental language disorders. Hove and New York: Psychology Press.

    Google Scholar 

  88. Norbury, C.F., Gooch, D., Wray, C., Baird, G., Charmand, T., Simonoff, E., … & Andrew, P. (2016). The impact of NVIQ on prevalence and clinical presentation of language disorder: evidence from a population study. Journal of Child Psychology and Psychiatry, 11, 1247–1257.

  89. Norrelgen, F., Lacerda, F., & Forssberg, H. (2002). Temporal resolution of auditory perception and verbal working memory in 15 children with language impairment. Journal of Learning Disabilities, 35(6), 539–545.

    PubMed  Google Scholar 

  90. Oguz, I., Zhang, H., Rumple, A., & Sonka, M. (2014). RATS: Rapid automatic tissue segmentation in rodent brain MRI. Journal of Neuroscience Methods, 221, 175–182.

    PubMed  Google Scholar 

  91. Ortibus, E., Verhoeven, J., Sunaert, S., Casteels, I., de Cock, P., & Lagae, L. (2012). Integrity of the inferior longitudinal fasciculus and impaired object recognition in children: a diffusion tensor imaging study. Developmental Medicine and Child Neurology, 54(1), 38–43.

    PubMed  Google Scholar 

  92. Partanen, E., Kujala, T., Naatanen, R., Liitola, A., Sambeth, A., & Huotilainen, M. (2013). Learning-induced neural plasticity of speech processing before birth. PNAS, 110(37), 15145–15150.

    CAS  PubMed  Google Scholar 

  93. Perani, D., Saccuman, M. C., Scifo, P., Anwander, A., Spada, D., Baldoli, C., et al. (2011). Neural language networks at birth. PNAS, 108(38), 16056–16061.

    CAS  PubMed  Google Scholar 

  94. Plante, E., Swisher, L., Vance, R., & Rapcsak, S. (1991). MRI findings in boys with specific language impairment. Brain and Language, 41, 52–66.

    CAS  PubMed  Google Scholar 

  95. Poll, G. H. (2011). Increasing the odds: applying emergentist theory in language intervention. Language, Speech, and Hearing Services in Schools, 42(4), 580–591. https://doi.org/10.1044/0161-1461(2011/10-0041).

    Article  PubMed  PubMed Central  Google Scholar 

  96. Preis, S., Steinmetz, H., Knorr, U., & Jancke, L. (2000). Corpus callosum size in children with developmental language disorder. Brain Research Cognitive Brain Research, 10(1–2), 37–44.

    CAS  PubMed  Google Scholar 

  97. Qiu, A., Mori, S., & Miller, M. I. (2015). Diffusion tensor imaging for understanding brain development in early life. Annual Review of Psychology, 66, 853–576.

    PubMed  PubMed Central  Google Scholar 

  98. Roberts, T. P. L., Heiken, K., Zarnow, D., Dell, J., Nagae, L., Blaskey, L., … Edgar, J. C. (2014). Left hemisphere diffusivity of the arcuate fasciculus: influences of autism spectrum disorder and language impairment. American Journal of Neuroradiology, 35(3), 587–592.

  99. Rolheiser, T., Stamatakis, E. A., & Tyler, L. K. (2011). Dynamic processing in the human language system: synergy between the arcuate fascicle and extreme capsule. The Journal of Neuroscience, 31(47), 16949–16957.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Saur, D., Kreher, B. W., Schnell, S., Kummerer, D., Kellmeyer, P., Vry, M., et al. (2008). Ventral and dorsal pathways for language. PNAS, 105(46), 18035–18040.

    CAS  PubMed  Google Scholar 

  101. Semel, E. M., Wiig, E. H., & Secord, W. (2003). Clinical evaluation of language fundamentals, fourth edition (CELF-4). San Antonio: The Psychological Corporation.

    Google Scholar 

  102. Shinoura, N., Suzuki, Y., Tsukada, M., Katsuki, S., Yamada, R., Tabei, Y., et al. (2007). Impairment of inferior longitudinal fasciculus plays a role in visual memory disturbance. Neurocase, 13(2), 127–139.

    PubMed  Google Scholar 

  103. Simmonds, D., Hallquist, M. N., Asato, M., & Luna, B. (2014). Developmental stages and sex differences of white matter and behavioral development through adolescence: a longitudinal diffusion tensor imaging (DTI) Study. NeuroImage, 92, 356–368.

    PubMed  Google Scholar 

  104. Soriano-Mas, C., Pujol, J., Ortiz, H., Deus, J., Lopez-Sala, A., & Sans, A. (2009). Age-related brain structural alterations in children with specific language impairment. Human Brain Mapping, 30(5), 1626–1636.

    PubMed  Google Scholar 

  105. Tallal, P., Miller, S. L., Jenkins, W. M., & Merzenich, M. M. (1997). The role of temporal processing in developmental language-based learning disorders: Research and clinical implications. In B. A. Blachman (Ed.), Foundations of reading acquisition and dyslexia: Implications for early intervention (pp. 49–66). Mahwah: Lawrence Erlbaum.

    Google Scholar 

  106. Thomas, M., & Karmiloff-Smith, A. (2002). Are developmental disorders like cases of adult brain damage? Implications from connectionist modelling. Behavioral and Brain Sciences, 25(6), 727–750.

    PubMed  Google Scholar 

  107. Tomblin, J. B. (2008). Validating diagnostic standards for specific language impairment using adolescent outcomes. In C. F. Norbury, J. B. Tomblin, & D. V. Bishop (Eds.), Understanding developmental language disorders (pp. 93–114). Hove and New York: Psychology Press.

    Google Scholar 

  108. Tomblin, J. B., & Christiansen, M. H. (2010). Explaining developmental communication disorders. In R. Paul & P. Flipsen Jr. (Eds.), Speech sound disorders in children: In honor of Lawrence D. Shriberg (pp. 35–49). San Diego, CA: Plural Publishing.

    Google Scholar 

  109. Tomblin, J. B., & Zhang, X. (2006). The dimensionality of language ability in school-age children. Journal of Speech, Language, and Hearing Research, 49(6), 1193–1208.

    PubMed  Google Scholar 

  110. Tomblin, J. B., Records, N. L., & Zhang, X. (1996). A system for the diagnosis of specific language impairment in kindergarten children. Journal of Speech and Hearing Research, 39, 1284–1294.

    CAS  PubMed  Google Scholar 

  111. Tomblin, J. B., Records, N. L., Buckwalter, P., Zhang, X., Smith, E., & O’Brien, M. (1997). Prevalence of specific language impairment in kindergarten children. Journal of Speech and Hearing Research, 40(6), 1245–1260.

    CAS  Google Scholar 

  112. Urger, S. E., de Bellis, M. D., Hooper, S. R., Woolley, D. P., Chen, S. D., & Provenzale, J. (2015). The superior longitudinal fasciculus in typically developing children and adolescents. Journal of Child Neurology, 30(1), 9–20.

    PubMed  Google Scholar 

  113. Verhoeven, J. S., Rommel, N., Prodi, E., Leemans, A., Zink, I., Vandewalle, E., … Sunaert, S. (2012). Is there a common neuroanatomical substrate of language deficit between autism spectrum disorder and specific language impairment? Cerebral Cortex, 22(10), 2263–2271.

  114. Verly, M., Gerrits, R., Sleurs, C., Lagae, L., Sunaert, S., Zink, I., & Rommel, N. (2018). The mis-wired language network in children with developmental language disorder: insights from DTI tractography. Brain Imaging and Behavior. https://doi.org/10.1007/s11682-018-9903-3.

  115. Vissers, C., Koolen, S., Hermans, D., Scheper, A., & Knoors, H. (2015). Executive functioning in preschoolers with specific language impairment. Frontiers in Psychology, 20(6), 1574.

    Google Scholar 

  116. Vydrova, R., Komarek, V., Sanda, J., Sterbova, K., Jahodova, A., Maulisova, A., et al. (2015). Structural alterations of the language connectome in children with specific language impairment. Brain and Language, 151, 35–41.

    PubMed  Google Scholar 

  117. Wakana, S., Caprihan, A., Panzenboeck, M. M., Fallon, J. H., Perry, M., Gollub, R. L., … Mori, S. (2007). Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage, 36(3), 630–644.

  118. Wechsler, D. (1999). Wechsler abbreviated scale of intelligence (WASI). San Antonio: The Psychological Corporation.

    Google Scholar 

  119. Westermann, G. (2016). Experience-dependent brain development as a key to understanding the language system. Topics in Cognitive Science, 8(2), 446–458.

    PubMed  Google Scholar 

  120. Wiecki, T. V., & Frank, M. J. (2013). A computational model of inhibitory control in frontal cortex and basal ganglia. Psychological Review, 120(2), 329–355.

    PubMed  Google Scholar 

  121. Williams, K. (1997). Expressive vocabulary test, second edition (EVT-2). Circle Pines: American Guidance Service.

    Google Scholar 

  122. Wilson, S. M., Galantucci, S., Tartaglia, M. C. R. K., Patterson, D. K., Henry, M. L., … Gorno-Tempini, M. L. (2011). Syntactic processing depends on dorsal language tracts. Neuron, 72(2), 397–403.

  123. Wong, F. C. K., Chandrasekaran, B., Garibaldi, K., & Wong, P. C. M. (2011). White matter anisotropy in the ventral language pathway predicts sound-to-word learning success. Journal of Neuroscience, 31(24), 8780–8785.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the staff in the Child Language Research Center and the MACLab at the University of Iowa for their help with subject recruitment and data collection, as well as Eric Axelson in the Nopoulos Lab for his assistance in image preprocessing and processing. We also want to express our gratitude to our participants and their parents for agreeing to take part in this study.

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Correspondence to Joanna C. Lee.

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This work was supported by the National Institute on Deafness and Other Communication Disorders (NIDCD) awarded to Dr. Tomblin [Grant R21DC013733]. All authors declare that they have no conflict of interest. All procedures performed in the study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.

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Lee, J.C., Dick, A.S. & Tomblin, J.B. Altered brain structures in the dorsal and ventral language pathways in individuals with and without developmental language disorder (DLD). Brain Imaging and Behavior 14, 2569–2586 (2020). https://doi.org/10.1007/s11682-019-00209-1

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Keywords

  • Developmental language disorder
  • Dorsal pathway
  • Ventral pathway
  • Structural brain imaging