Altered structural brain connectivity involving the dorsal and ventral language pathways in 16p11.2 deletion syndrome

Original Research
  • 31 Downloads

Abstract

Copy number variants at the chromosomal locus 16p11.2 contribute to neurodevelopmental disorders such as autism spectrum disorders, epilepsy, schizophrenia, and language and articulation disorders. Here, we provide detailed findings on the disrupted structural brain connectivity in 16p11.2 deletion syndrome (patients: N = 21, age range: 8–16 years; typically developing (TD) controls: 18, 9–16 years) using structural and diffusion MRI. We performed global short-, middle-, long-range, and interhemispheric connectivity analysis in the whole brain using gyral topology-based cortical parcellation. Using region of interest analysis, we studied bilateral dorsal (3 segments of arcuate fasciculus (AF)) and ventral (inferior fronto-occipital fasciculus (IFOF), inferior longitudinal fasciculus (ILF), uncinate fasciculus (UF)) language pathways. Our results showed significantly increased axial (AD) and radial (RD) diffusivities in bilateral anterior AF, decreased volume for left long AF, increased mean diffusivity (MD) and RD for right long AF, and increased AD for bilateral UF in the 16p11.2 deletion group in the absence of significant abnormalities in the whole-brain gyral and interhemispheric connectivity. The selective involvement of the language networks may aid in understanding effects of altered white matter connectivity on neurodevelopmental outcomes in 16p11.2 deletion.

Keywords

16p11.2 deletion Brain networks Diffusion tensor imaging Language pathways Autism 

Notes

Acknowledgements

This work is submitted on behalf of the Simons Variation in Individuals Project (Simons VIP) investigators. We are grateful to all off the families at the participating Simons Variation in Individuals Project (Simons VIP) sites, as well as the investigators in the Simons VIP Consortium (Simons VIP Consortium, 2012). We are thankful to be given access to the phenotypic data on SFARI Base. We would also like to acknowledge Marie Drottar and Ashley Curran for their assistance.

Compliance with ethical standards

Conflict of interest

Authors Banu Ahtam, Naira Link, Erikson Hoff, P. Ellen Grant, and Kiho Im declare that they have no conflict of interest.

Ethics approval

All procedures performed in studies 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

Informed consent was obtained from all individual participants included in the study.

Supplementary material

11682_2018_9859_MOESM1_ESM.docx (179 kb)
Supplementary Table 1 (DOCX 179 kb)

References

  1. Almairac, F., Herbet, G., Moritz-Gasser, S., de Champfleur, N. M., & Duffau, H. (2015). The left inferior fronto-occipital fasciculus subserves language semantics: A multilevel lesion study. Brain Structure & Function, 220, 1983–1995.CrossRefGoogle Scholar
  2. Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31, 137–145.CrossRefPubMedGoogle Scholar
  3. Basilakos, A., Fillmore, P. T., Rorden, C., Guo, D., Bonilha, L., & Fridriksson, J. (2014). Regional white matter damage predicts speech fluency in chronic post-stroke aphasia. Frontiers in Human Neuroscience, 8, 845.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Berman, J. I., Chudnovskaya, D., Blaskey, L., Kuschner, E., Mukherjee, P., Buckner, R., Nagarajan, S., Chung, W. K., Spiro, J. E., Sherr, E. H., & Roberts, T. P. (2015). Abnormal auditory and language pathways in children with 16p11.2 deletion. Neuroimage Clinics, 9, 50–57.CrossRefGoogle Scholar
  5. Berman, J. I., Chudnovskaya, D., Blaskey, L., Kuschner, E., Mukherjee, P., Buckner, R., Nagarajan, S., Chung, W. K., Sherr, E. H., & Roberts, T. P. (2016). Relationship between M100 auditory evoked response and auditory radiation microstructure in 16p11.2 deletion and duplication carriers. AJNR. American Journal of Neuroradiology, 37, 1178–1184.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Billeci, L., Calderoni, S., Tosetti, M., Catani, M., & Muratori, F. (2012). White matter connectivity in children with autism spectrum disorders: A tract-based spatial statistics study. BMC Neurology, 12, 148.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Blackmon, K., Thesen, T., Green, S., Ben-Avi, E., Wang, X., Fuchs, B., Kuzniecky, R., & Devinsky, O. (2017). Focal cortical anomalies and language impairment in 16p11.2 deletion and duplication syndrome. Cerebral Cortex, 1–9.  https://doi.org/10.1093/cercor/bhx143
  8. Bloemen, O. J., Deeley, Q., Sundram, F., Daly, E. M., Barker, G. J., Jones, D. K., van Amelsvoort, T. A., Schmitz, N., Robertson, D., Murphy, K. C., & Murphy, D. G. (2010). White matter integrity in Asperger syndrome: A preliminary diffusion tensor magnetic resonance imaging study in adults. Autism Research, 3, 203–213.CrossRefPubMedGoogle Scholar
  9. Budde, M. D., Xie, M., Cross, A. H., & Song, S. K. (2009). Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: A quantitative pixelwise analysis. The Journal of Neuroscience, 29, 2805–2813.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Catani, M., & Mesulam, M. (2008). The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state. Cortex, 44, 953–961.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Catani, M., Jones, D. K., & ffytche, D. H. (2005). Perisylvian language networks of the human brain. Annals of Neurology, 57, 8–16.CrossRefPubMedGoogle Scholar
  12. Catani, M., Allin, M. P., Husain, M., Pugliese, L., Mesulam, M. M., Murray, R. M., & Jones, D. K. (2007). Symmetries in human brain language pathways correlate with verbal recall. Proceedings of the National Academy of Sciences of the United States of America, 104, 17163–17168.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Catani, M., Craig, M. C., Forkel, S. J., Kanaan, R., Picchioni, M., Toulopoulou, T., Shergill, S., Williams, S., Murphy, D. G., & McGuire, P. (2011). Altered integrity of perisylvian language pathways in schizophrenia: Relationship to auditory hallucinations. Biological Psychiatry, 70, 1143–1150.CrossRefPubMedGoogle Scholar
  14. Chang, Y. S., Owen, J. P., Pojman, N. J., Thieu, T., Bukshpun, P., Wakahiro, M. L., Marco, E. J., Berman, J. I., Spiro, J. E., Chung, W. K., Buckner, R. L., Roberts, T. P., Nagarajan, S. S., Sherr, E. H., & Mukherjee, P. (2016). Reciprocal white matter alterations due to 16p11.2 chromosomal deletions versus duplications. Human Brain Mapping, 37, 2833–2848.CrossRefPubMedGoogle Scholar
  15. Cheon, K. A., Kim, Y. S., Oh, S. H., Park, S. Y., Yoon, H. W., Herrington, J., Nair, A., Koh, Y. J., Jang, D. P., Kim, Y. B., Leventhal, B. L., Cho, Z. H., Castellanos, F. X., & Schultz, R. T. (2011). Involvement of the anterior thalamic radiation in boys with high functioning autism spectrum disorders: A diffusion tensor imaging study. Brain Research, 1417, 77–86.CrossRefPubMedGoogle Scholar
  16. Curcic-Blake, B., Nanetti, L., van der Meer, L., Cerliani, L., Renken, R., Pijnenborg, G. H., & Aleman, A. (2015). Not on speaking terms: Hallucinations and structural network disconnectivity in schizophrenia. Brain Structure & Function, 220, 407–418.CrossRefGoogle Scholar
  17. Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9, 179–194.CrossRefPubMedGoogle Scholar
  18. Desikan, R. S., Segonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. L., Dale, A. M., Maguire, R. P., Hyman, B. T., Albert, M. S., & Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31, 968–980.CrossRefPubMedGoogle Scholar
  19. Dick, A. S., & Tremblay, P. (2012). Beyond the arcuate fasciculus: Consensus and controversy in the connectional anatomy of language. Brain, 135, 3529–3550.CrossRefPubMedGoogle Scholar
  20. Duffau, H., Gatignol, P., Mandonnet, E., Peruzzi, P., Tzourio-Mazoyer, N., & Capelle, L. (2005). New insights into the anatomo-functional connectivity of the semantic system: A study using cortico-subcortical electrostimulations. Brain, 128, 797–810.CrossRefPubMedGoogle Scholar
  21. Elliott, C. D. (2007). Differential ability scales (2nd Ed.) Canadian Journal of School Psychology, 22, 128–132.CrossRefGoogle Scholar
  22. Epstein, K. A., Cullen, K. R., Mueller, B. A., Robinson, P., Lee, S., & Kumra, S. (2014). White matter abnormalities and cognitive impairment in early-onset schizophrenia-spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 53(362–372), e361–e362.Google Scholar
  23. Fischl, B., Sereno, M. I., & Dale, A. M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage, 9, 195–207.CrossRefPubMedGoogle Scholar
  24. Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., van der Kouwe, A., Killiany, R., Kennedy, D., Klaveness, S., Montillo, A., Makris, N., Rosen, B., & Dale, A. M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341–355.CrossRefPubMedGoogle Scholar
  25. Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D. H., Busa, E., Seidman, L. J., Goldstein, J., Kennedy, D., Caviness, V., Makris, N., Rosen, B., & Dale, A. M. (2004a). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11–22.CrossRefPubMedGoogle Scholar
  26. Fischl, B., Salat, D. H., van der Kouwe, A. J., Makris, N., Segonne, F., Quinn, B. T., & Dale, A. M. (2004b). Sequence-independent segmentation of magnetic resonance images. NeuroImage, 23(Suppl 1), S69–S84.CrossRefPubMedGoogle Scholar
  27. Fletcher, P. T., Whitaker, R. T., Tao, R., DuBray, M. B., Froehlich, A., Ravichandran, C., Alexander, A. L., Bigler, E. D., Lange, N., & Lainhart, J. E. (2010). Microstructural connectivity of the arcuate fasciculus in adolescents with high-functioning autism. NeuroImage, 51, 1117–1125.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Frey, S., Kostopoulos, P., & Petrides, M. (2004). Orbitofrontal contribution to auditory encoding. NeuroImage, 22, 1384–1389.CrossRefPubMedGoogle Scholar
  29. Fridriksson, J., Guo, D., Fillmore, P., Holland, A., & Rorden, C. (2013). Damage to the anterior arcuate fasciculus predicts non-fluent speech production in aphasia. Brain, 136, 3451–3460.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Grossman, M., McMillan, C., Moore, P., Ding, L., Glosser, G., Work, M., & Gee, J. (2004). What's in a name: Voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer's disease, frontotemporal dementia and corticobasal degeneration. Brain, 127, 628–649.CrossRefPubMedGoogle Scholar
  31. Hanson, E., Nasir, R. H., Fong, A., Lian, A., Hundley, R., Shen, Y., Wu, B. L., Holm, I. A., Miller, D. T., & p11.2 Study Group C. (2010). Cognitive and behavioral characterization of 16p11.2 deletion syndrome. Journal of Developmental and Behavioral Pediatrics, 31, 649–657.CrossRefPubMedGoogle Scholar
  32. Hanson, E., Bernier, R., Porche, K., Jackson, F. I., Goin-Kochel, R. P., Snyder, L. G., Snow, A. V., Wallace, A. S., Campe, K. L., Zhang, Y., Chen, Q., D'Angelo, D., Moreno-De-Luca, A., Orr, P. T., Boomer, K. B., Evans, D. W., Kanne, S., Berry, L., Miller, F. K., Olson, J., Sherr, E., Martin, C. L., Ledbetter, D. H., Spiro, J. E., Chung, W. K., & Simons Variation in Individuals Project C. (2015). The cognitive and behavioral phenotype of the 16p11.2 deletion in a clinically ascertained population. Biological Psychiatry, 77, 785–793.CrossRefPubMedGoogle Scholar
  33. Hickok, G., & Poeppel, D. (2004). Dorsal and ventral streams: A framework for understanding aspects of the functional anatomy of language. Cognition, 92, 67–99.CrossRefPubMedGoogle Scholar
  34. Hickok, G., & Poeppel, D. (2007). The cortical organization of speech processing. Nature Reviews. Neuroscience, 8, 393–402.CrossRefPubMedGoogle Scholar
  35. Im, K., Paldino, M. J., Poduri, A., Sporns, O., & Grant, P. E. (2014). Altered white matter connectivity and network organization in polymicrogyria revealed by individual gyral topology-based analysis. NeuroImage, 86, 182–193.CrossRefPubMedGoogle Scholar
  36. Im, K., Ahtam, B., Haehn, D., Peters, J. M., Warfield, S. K., Sahin, M., & Ellen Grant, P. (2016). Altered structural brain networks in tuberous sclerosis complex. Cerebral Cortex, 26, 2046–2058.CrossRefPubMedGoogle Scholar
  37. Jenkins 3rd, J., Chow, V., Blaskey, L., Kuschner, E., Qasmieh, S., Gaetz, L., Edgar, J. C., Mukherjee, P., Buckner, R., Nagarajan, S. S., Chung, W. K., Spiro, J. E., Sherr, E. H., Berman, J. I., & Roberts, T. P. (2016). Auditory evoked M100 response latency is delayed in children with 16p11.2 deletion but not 16p11.2 duplication. Cerebral Cortex, 26, 1957–1964.CrossRefPubMedGoogle Scholar
  38. Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5, 143–156.CrossRefPubMedGoogle Scholar
  39. Jenkinson, M., Bannister, P., Brady, M., & Smith, S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage, 17, 825–841.CrossRefPubMedGoogle Scholar
  40. Jou, R. J., Jackowski, A. P., Papademetris, X., Rajeevan, N., Staib, L. H., & Volkmar, F. R. (2011). Diffusion tensor imaging in autism spectrum disorders: Preliminary evidence of abnormal neural connectivity. The Australian and New Zealand Journal of Psychiatry, 45, 153–162.CrossRefPubMedGoogle Scholar
  41. Kang, H. J., Kawasawa, Y. I., Cheng, F., Zhu, Y., Xu, X., Li, M., Sousa, A. M., Pletikos, M., Meyer, K. A., Sedmak, G., Guennel, T., Shin, Y., Johnson, M. B., Krsnik, Z., Mayer, S., Fertuzinhos, S., Umlauf, S., Lisgo, S. N., Vortmeyer, A., Weinberger, D. R., Mane, S., Hyde, T. M., Huttner, A., Reimers, M., Kleinman, J. E., & Sestan, N. (2011). Spatio-temporal transcriptome of the human brain. Nature, 478, 483–489.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kepinska, O., Lakke, E., Dutton, E. M., Caspers, J., & Schiller, N. O. (2017). The perisylvian language network and language analytical abilities. Neurobiology of Learning and Memory, 144, 96–101.CrossRefPubMedGoogle Scholar
  43. Knaus, T. A., Silver, A. M., Kennedy, M., Lindgren, K. A., Dominick, K. C., Siegel, J., & Tager-Flusberg, H. (2010). Language laterality in autism spectrum disorder and typical controls: A functional, volumetric, and diffusion tensor MRI study. Brain and Language, 112, 113–120.CrossRefPubMedGoogle Scholar
  44. Kumar, R., Macey, P. M., Woo, M. A., Alger, J. R., & Harper, R. M. (2008). Diffusion tensor imaging demonstrates brainstem and cerebellar abnormalities in congenital central hypoventilation syndrome. Pediatric Research, 64, 275–280.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lange, N., Dubray, M. B., Lee, J. E., Froimowitz, M. P., Froehlich, A., Adluru, N., Wright, B., Ravichandran, C., Fletcher, P. T., Bigler, E. D., Alexander, A. L., & Lainhart, J. E. (2010). Atypical diffusion tensor hemispheric asymmetry in autism. Autism Research, 3, 350–358.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lewis, W. W., Sahin, M., Scherrer, B., Peters, J. M., Suarez, R. O., Vogel-Farley, V. K., Jeste, S. S., Gregas, M. C., Prabhu, S. P., Nelson 3rd, C. A., & Warfield, S. K. (2013). Impaired language pathways in tuberous sclerosis complex patients with autism spectrum disorders. Cerebral Cortex, 23, 1526–1532.CrossRefPubMedGoogle Scholar
  47. Lopez-Barroso, D., Catani, M., Ripolles, P., Dell'Acqua, F., Rodriguez-Fornells, A., & de Diego-Balaguer, R. (2013). Word learning is mediated by the left arcuate fasciculus. Proceedings of the National Academy of Sciences of the United States of America, 110, 13168–13173.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Lu, L. H., Crosson, B., Nadeau, S. E., Heilman, K. M., Gonzalez-Rothi, L. J., Raymer, A., Gilmore, R. L., Bauer, R. M., & Roper, S. N. (2002). Category-specific naming deficits for objects and actions: Semantic attribute and grammatical role hypotheses. Neuropsychologia, 40, 1608–1621.CrossRefPubMedGoogle Scholar
  49. Ly, M. T., Nanavati, T. U., Frum, C. A., & Pergami, P. (2015). Comparing tract-based spatial statistics and manual region-of-interest labeling as diffusion analysis methods to detect white matter abnormalities in infants with hypoxic-ischemic encephalopathy. Journal of Magnetic Resonance Imaging, 42, 1689–1697.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Maillard, A. M., Ruef, A., Pizzagalli, F., Migliavacca, E., Hippolyte, L., Adaszewski, S., Dukart, J., Ferrari, C., Conus, P., Mannik, K., Zazhytska, M., Siffredi, V., Maeder, P., Kutalik, Z., Kherif, F., Hadjikhani, N., Beckmann, J. S., Reymond, A., Draganski, B., Jacquemont, S., & p11.2 European C. (2015). The 16p11.2 locus modulates brain structures common to autism, schizophrenia and obesity. Molecular Psychiatry, 20, 140–147.CrossRefPubMedGoogle Scholar
  51. 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, 623–629.CrossRefPubMedGoogle Scholar
  52. Markou, P., Ahtam, B., & Papadatou-Pastou, M. (2017). Elevated levels of atypical handedness in autism: Meta-analyses. Neuropsychology Review, 27, 258–283.CrossRefPubMedGoogle Scholar
  53. Mills, B. D., Lai, J., Brown, T. T., Erhart, M., Halgren, E., Reilly, J., Dale, A., Appelbaum, M., & Moses, P. (2013). White matter microstructure correlates of narrative production in typically developing children and children with high functioning autism. Neuropsychologia, 51, 1933–1941.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Mori, S., Crain, B. J., Chacko, V. P., & van Zijl, P. C. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annals of Neurology, 45, 265–269.CrossRefPubMedGoogle Scholar
  55. Moseley, R. L., Correia, M. M., Baron-Cohen, S., Shtyrov, Y., Pulvermuller, F., & Mohr, B. (2016). Reduced volume of the arcuate fasciculus in adults with high-functioning autism Spectrum conditions. Frontiers in Human Neuroscience, 10, 214.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nagae, L. M., Zarnow, D. M., Blaskey, L., Dell, J., Khan, S. Y., Qasmieh, S., Levy, S. E., & Roberts, T. P. (2012). Elevated mean diffusivity in the left hemisphere superior longitudinal fasciculus in autism spectrum disorders increases with more profound language impairment. AJNR. American Journal of Neuroradiology, 33, 1720–1725.CrossRefPubMedGoogle Scholar
  57. Oishi, K., Faria, A. V., Hsu, J., Tippett, D., Mori, S., & Hillis, A. E. (2015). Critical role of the right uncinate fasciculus in emotional empathy. Annals of Neurology, 77, 68–74.CrossRefPubMedGoogle Scholar
  58. Olson, I. R., Von Der Heide, R. J., Alm, K. H., & Vyas, G. (2015). Development of the uncinate fasciculus: Implications for theory and developmental disorders. Developmental Cognitive Neuroscience, 14, 50–61.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Owen, J. P., Chang, Y. S., Pojman, N. J., Bukshpun, P., Wakahiro, M. L., Marco, E. J., Berman, J. I., Spiro, J. E., Chung, W. K., Buckner, R. L., Roberts, T. P., Nagarajan, S. S., Sherr, E. H., Mukherjee, P., & Simons, V. I. P. C. (2014). Aberrant white matter microstructure in children with 16p11.2 deletions. The Journal of Neuroscience, 34, 6214–6223.CrossRefPubMedGoogle Scholar
  60. Owen, J. P., Bukshpun, P., Pojman, N., Thieu, T., Chen, Q., Lee, J., D'Angelo, D., Glenn, O. A., Hunter, J. V., Berman, J. I., Roberts, T. P., Buckner, R., Nagarajan, S. S., Mukherjee, P., & Sherr, E. H. (2018). Brain MR imaging findings and associated outcomes in carriers of the reciprocal copy number variation at 16p11.2. Radiology, 286, 217–226.Google Scholar
  61. Parker, G. J., Luzzi, S., Alexander, D. C., Wheeler-Kingshott, C. A., Ciccarelli, O., & Lambon Ralph, M. A. (2005). Lateralization of ventral and dorsal auditory-language pathways in the human brain. NeuroImage, 24, 656–666.CrossRefPubMedGoogle Scholar
  62. Peters, J. M., Sahin, M., Vogel-Farley, V. K., Jeste, S. S., Nelson 3rd, C. A., Gregas, M. C., Prabhu, S. P., Scherrer, B., & Warfield, S. K. (2012). Loss of white matter microstructural integrity is associated with adverse neurological outcome in tuberous sclerosis complex. Academic Radiology, 19, 17–25.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pugliese, L., Catani, M., Ameis, S., Dell'Acqua, F., Thiebaut de Schotten, M., Murphy, C., Robertson, D., Deeley, Q., Daly, E., & Murphy, D. G. (2009). The anatomy of extended limbic pathways in Asperger syndrome: A preliminary diffusion tensor imaging tractography study. NeuroImage, 47, 427–434.CrossRefPubMedGoogle Scholar
  64. Qureshi, A. Y., Mueller, S., Snyder, A. Z., Mukherjee, P., Berman, J. I., Roberts, T. P., Nagarajan, S. S., Spiro, J. E., Chung, W. K., Sherr, E. H., Buckner, R. L., & Simons, V. I. P. C. (2014). Opposing brain differences in 16p11.2 deletion and duplication carriers. The Journal of Neuroscience, 34, 11199–11211.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Rane, P., Cochran, D., Hodge, S. M., Haselgrove, C., Kennedy, D. N., & Frazier, J. A. (2015). Connectivity in autism: A review of MRI connectivity studies. Harvard Review of Psychiatry, 23, 223–244.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Roberts, T. P., Heiken, K., Zarnow, D., Dell, J., Nagae, L., Blaskey, L., Solot, C., Levy, S. E., Berman, J. I., & Edgar, J. C. (2014). Left hemisphere diffusivity of the arcuate fasciculus: Influences of autism spectrum disorder and language impairment. AJNR. American Journal of Neuroradiology, 35, 587–592.CrossRefPubMedGoogle Scholar
  67. Rosenfeld, J. A., Coppinger, J., Bejjani, B. A., Girirajan, S., Eichler, E. E., Shaffer, L. G., & Ballif, B. C. (2010). Speech delays and behavioral problems are the predominant features in individuals with developmental delays and 16p11.2 microdeletions and microduplications. Journal of Neurodevelopmental Disorders, 2, 26–38.CrossRefPubMedGoogle Scholar
  68. Sahyoun, C. P., Belliveau, J. W., & Mody, M. (2010). White matter integrity and pictorial reasoning in high-functioning children with autism. Brain and Cognition, 73, 180–188.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Saur, D., Kreher, B. W., Schnell, S., Kummerer, D., Kellmeyer, P., Vry, M. S., Umarova, R., Musso, M., Glauche, V., Abel, S., Huber, W., Rijntjes, M., Hennig, J., & Weiller, C. (2008). Ventral and dorsal pathways for language. Proceedings of the National Academy of Sciences of the United States of America, 105, 18035–18040.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Semel E, Wiig EH, Secord WA. 2003. Clinical evaluation of language fundamentals, fourth edition (CELF-4). Toronto: Canada: The Psychological Corporation/A Harcourt Assessment Company.Google Scholar
  71. Shukla, D. K., Keehn, B., Smylie, D. M., & Muller, R. A. (2011a). Microstructural abnormalities of short-distance white matter tracts in autism spectrum disorder. Neuropsychologia, 49, 1378–1382.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Shukla, D. K., Keehn, B., & Muller, R. A. (2011b). Tract-specific analyses of diffusion tensor imaging show widespread white matter compromise in autism spectrum disorder. Journal of Child Psychology and Psychiatry, 52, 286–295.CrossRefPubMedGoogle Scholar
  73. Simons Vip, C. (2012). Simons variation in individuals project (Simons VIP): A genetics-first approach to studying autism spectrum and related neurodevelopmental disorders. Neuron, 73, 1063–1067.CrossRefGoogle Scholar
  74. Singh, S., Singh, K., Trivedi, R., Goyal, S., Kaur, P., Singh, N., Bhatia, T., Deshpande, S. N., & Khushu, S. (2016). Microstructural abnormalities of uncinate fasciculus as a function of impaired cognition in schizophrenia: A DTI study. Journal of Biosciences, 41, 419–426.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., Watkins, K. E., Ciccarelli, O., Cader, M. Z., Matthews, P. M., & Behrens, T. E. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. NeuroImage, 31, 1487–1505.CrossRefPubMedGoogle Scholar
  76. Song, S. K., Sun, S. W., Ju, W. K., Lin, S. J., Cross, A. H., & Neufeld, A. H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage, 20, 1714–1722.CrossRefPubMedGoogle Scholar
  77. Steinman, K. J., Spence, S. J., Ramocki, M. B., Proud, M. B., Kessler, S. K., Marco, E. J., Green Snyder, L., D'Angelo, D., Chen, Q., Chung, W. K., Sherr, E. H., & Simons, V. I. P. C. (2016). 16p11.2 deletion and duplication: Characterizing neurologic phenotypes in a large clinically ascertained cohort. American Journal of Medical Genetics. Part A, 170, 2943–2955.CrossRefPubMedGoogle Scholar
  78. Takahashi, E., Folkerth, R. D., Galaburda, A. M., & Grant, P. E. (2012). Emerging cerebral connectivity in the human fetal brain: An MR tractography study. Cerebral Cortex, 22, 455–464.CrossRefPubMedGoogle Scholar
  79. Takahashi, E., Hayashi, E., Schmahmann, J. D., & Grant, P. E. (2014). Development of cerebellar connectivity in human fetal brains revealed by high angular resolution diffusion tractography. NeuroImage, 96, 326–333.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Thiebaut de Schotten, M., Ffytche, D. H., Bizzi, A., Dell'Acqua, F., Allin, M., Walshe, M., Murray, R., Williams, S. C., Murphy, D. G., & Catani, M. (2011). Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. NeuroImage, 54, 49–59.CrossRefPubMedGoogle Scholar
  81. Travers, B. G., Adluru, N., Ennis, C., Tromp do, P. M., Destiche, D., Doran, S., Bigler, E. D., Lange, N., Lainhart, J. E., & Alexander, A. L. (2012). Diffusion tensor imaging in autism spectrum disorder: A review. Autism Research, 5, 289–313.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Turken, A. U., & Dronkers, N. F. (2011). The neural architecture of the language comprehension network: Converging evidence from lesion and connectivity analyses. Frontiers in Systems Neuroscience, 5, 1.CrossRefPubMedPubMedCentralGoogle Scholar
  83. Verly, M., Verhoeven, J., Zink, I., Mantini, D., Van Oudenhove, L., Lagae, L., Sunaert, S., & Rommel, N. (2014). Structural and functional underconnectivity as a negative predictor for language in autism. Human Brain Mapping, 35, 3602–3615.CrossRefPubMedGoogle Scholar
  84. Vydrova, R., Komarek, V., Sanda, J., Sterbova, K., Jahodova, A., Maulisova, A., Zackova, J., Reissigova, J., Krsek, P., & Kyncl, M. (2015). Structural alterations of the language connectome in children with specific language impairment. Brain and Language, 151, 35–41.CrossRefPubMedGoogle Scholar
  85. Wagner RK, Torgesen JK, Rashotte CA. 1999. Comprehensive Test of Phonological Processing. Austin, TX: Pro: Ed.Google Scholar
  86. Wan, C. Y., Marchina, S., Norton, A., & Schlaug, G. (2012). Atypical hemispheric asymmetry in the arcuate fasciculus of completely nonverbal children with autism. Annals of the New York Academy of Sciences, 1252, 332–337.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Wang, R., Benner, T., Sorensen, A., & Wedeen, V. (2007). Diffusion toolkit: a software package for diffusion imaging data processing and tractography. Proceedings on International Society for Magnetic Resonance in Medicine, 15, 3720.Google Scholar
  88. Wedeen, V. J., Wang, R. P., Schmahmann, J. D., Benner, T., Tseng, W. Y., Dai, G., Pandya, D. N., Hagmann, P., D'Arceuil, H., & de Crespigny, A. J. (2008). Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage, 41, 1267–1277.CrossRefPubMedGoogle Scholar
  89. Yendiki, A., Koldewyn, K., Kakunoori, S., Kanwisher, N., & Fischl, B. (2014). Spurious group differences due to head motion in a diffusion MRI study. NeuroImage, 88, 79–90.CrossRefPubMedGoogle Scholar
  90. Zikou, A. K., Xydis, V. G., Astrakas, L. G., Nakou, I., Tzarouchi, L. C., Tzoufi, M., & Argyropoulou, M. I. (2016). Diffusion tensor imaging in children with tuberous sclerosis complex: Tract-based spatial statistics assessment of brain microstructural changes. Pediatric Radiology, 46, 1158–1164.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Fetal-Neonatal Neuroimaging & Developmental Science Center, Boston Children’s HospitalHarvard Medical SchoolBostonUSA
  2. 2.Division of Newborn Medicine, Department of Medicine, Boston Children’s HospitalHarvard Medical SchoolBostonUSA
  3. 3.Division of Neuroradiology, Department of Radiology, Boston Children’s HospitalHarvard Medical SchoolBostonUSA

Personalised recommendations