Các dấu hiệu di truyền liên quan đến chứng khó đọc và rối loạn ngôn ngữ ảnh hưởng đến độ dày vỏ não và chất trắng ở trẻ em phát triển bình thường

Springer Science and Business Media LLC - Tập 10 Số 1 - Trang 272-282 - 2016
Eicher, John D.1, Montgomery, Angela M.2, Akshoomoff, Natacha3,4, Amaral, David G.5, Bloss, Cinnamon S.6, Libiger, Ondrej6, Schork, Nicholas J.6, Darst, Burcu F.6, Casey, B. J.7, Chang, Linda8, Ernst, Thomas8, Frazier, Jean9, Kaufmann, Walter E.10,11, Keating, Brian8, Kenet, Tal12, Kennedy, David9, Mostofsky, Stewart10, Murray, Sarah S.6, Sowell, Elizabeth R.13,14, Bartsch, Hauke15, Kuperman, Joshua M.15,16, Brown, Timothy T.3,15,16, Hagler, Donald J.15,17, Dale, Anders M.4,15,16,17,18, Jernigan, Terry L.3,4,17,18, Gruen, Jeffrey R.1,2,19,20
1Department of Genetics, Yale University, New Haven, USA
2Department of Pediatrics, Yale University School of Medicine, New Haven, USA
3Center for Human Development, University of California, San Diego, USA
4Department of Psychiatry, University of California, San Diego, USA
5Department of Psychiatry and Behavioral Sciences, University of California, Davis, USA
6Scripps Genomic Medicine, Scripps Health, Scripps Translational Science Institute, La Jolla, USA
7Sackler Institute for Developmental Psychobiology, Weil Cornell Medical College, New York, USA
8Department of Medicine, Queen’s Medical Center, University of Hawaii, Honolulu, USA
9Department of Psychiatry, University of Massachusetts Medical School, Boston, USA
10Kennedy Krieger Institute, Baltimore, USA
11Department of Neurology, Harvard Medical School, Children’s Hospital Boston, Boston, USA
12Department of Neurology and Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, USA
13Department of Pediatrics, University of Southern California, Los Angeles, USA
14Developmental Cognitive Neuroimaging Laboratory Children’s Hospital, Los Angeles, USA
15Multimodal Imaging Laboratory, University of California, San Diego, USA
16Department of Neurosciences, University of California, San Diego, USA
17Radiology, University of California, San Diego, USA
18Cognitive Science University of California, San Diego, USA
19Department of Investigative, School of Medicine, Medicine Yale University, New Haven, USA
20Department of Pediatrics, Genetics, and Investigative Medicine, Yale Child Health Research Center, New Haven, USA

Tóm tắt

Chứng khó đọc và rối loạn ngôn ngữ (LI) là những đặc điểm phức tạp có thành phần di truyền đáng kể. Chúng tôi gần đây đã hoàn thành một cuộc quét liên kết ở vị trí DYX2, nơi chúng tôi đã quan sát thấy mối liên hệ của các dấu hiệu trong DCDC2, KIAA0319, ACOT13 và FAM65B với các đặc điểm liên quan đến đọc, ngôn ngữ và IQ. Ngoài ra, tác động của các dấu hiệu liên kết với việc đọc DYX3 đã được đặc trưng gần đây bằng cách sử dụng các kỹ thuật hình ảnh thần kinh cấu trúc. Ở đây, chúng tôi đã đánh giá các tác động hình ảnh thần kinh của các dấu hiệu liên kết DYX2 và DYX3, sử dụng thể tích vỏ não, độ dày vỏ não và độ bất đối xứng phân đoạn. Để thực hiện điều này, chúng tôi đã xem xét tám dấu hiệu DYX2 và ba dấu hiệu DYX3 trong 332 chủ thể trong nghiên cứu Di truyền Thần kinh Hình ảnh Trẻ em. Các mối liên kết hình ảnh-di truyền đã được kiểm tra bằng hồi quy tuyến tính đa biến, kiểm tra ảnh hưởng của kiểu gen đối với hình ảnh thần kinh. Các dấu hiệu trong các gen DYX2 KIAA0319 và FAM65B có liên quan đến độ dày vỏ não ở vùng vỏ trước trái và độ bất đối xứng phân đoạn toàn cầu, tương ứng. KIAA0319 và ACOT13 có nguy cơ liên kết với độ bất đối xứng phân đoạn tổng thể và độ dày vỏ não vùng trái pars opercularis, tương ứng. Các dấu hiệu DYX3 cho thấy các liên kết gợi ý với độ dày vỏ não và các chỉ số thể tích ở các vùng thời gian. Đáng chú ý, chúng tôi không tái tạo mối liên kết của các dấu hiệu DYX3 với các chỉ số hải mã. Tóm lại, chúng tôi đã thực hiện một cuộc theo dõi hình ảnh thần kinh về các dấu hiệu DYX2 và DYX3 liên quan đến đọc, ngôn ngữ và IQ. Các liên kết DYX2 với độ dày vỏ não có thể phản ánh sự khác biệt trong vai trò của chúng trong quá trình di chuyển neuron. Hơn nữa, phát hiện của chúng tôi bổ sung cho các nghiên cứu biểu hiện gen và hình ảnh cho thấy các dấu hiệu DYX3 ở các vùng thời gian. Những nghiên cứu này cung cấp cái nhìn về nơi và cách mà các biến thể nguy cơ DYX2 và DYX3 có thể ảnh hưởng đến các đặc điểm hình ảnh thần kinh. Các nghiên cứu trong tương lai nên kết nối thêm các con đường đến các biến thể nguy cơ liên quan đến kết quả hình ảnh/thần kinh nhận thức.

Từ khóa

#Dyslexia #Language Impairment #Neuroimaging #Cortical Thickness #DYX2 #DYX3

Tài liệu tham khảo

citation_journal_title=Neuropsychology; citation_title=The NIH toolbox cognition battery: results from a large normative developmental sample (PING); citation_author=N Akshoomoff, E Newman, WK Thompson, C McCabe, CS Bloss, L Chang, DG Amaral, BJ Casey, TM Ernst, JA Frazier, JR Gruen, WE Kaufmann, T Kenet, DN Kennedy, O Libiger, S Mostofsky, SS Murray, ER Sowell, N Schork, AM Dale, TL Jernigan; citation_volume=28; citation_issue=1; citation_publication_date=2014; citation_pages=1-10; citation_doi=10.1037/neu0000001; citation_id=CR1 citation_journal_title=Genome Research; citation_title=Fast model-based estimation of ancestry in unrelated individuals; citation_author=DH Alexander, J Novembre, K Lange; citation_volume=19; citation_issue=9; citation_publication_date=2009; citation_pages=1655-1664; citation_doi=10.1101/gr.094052.109; citation_id=CR2 citation_journal_title=Human Molecular Genetics; citation_title=A locus on 2p12 containing the co-regulated MRPL19 and C2orf3 genes is associated to dyslexia; citation_author=H Anthoni, M Zucchelli, H Matsson, B Müller-Myhsok, I Fransson, J Schumacher, S Massinen, P Onkamo, A Warnke, H Griesemann, P Hoffmann, J Nopola-Hemmi, H Lyytinen, G Schulte-Körne, J Kere, MM Nöthen, M Peyrard-Janvid; citation_volume=16; citation_issue=6; citation_publication_date=2007; citation_pages=667-677; citation_doi=10.1093/hmg/ddm009; citation_id=CR3 citation_journal_title=Bioinformatics; citation_title=Haploview: analysis and visualization of LD and haplotype maps; citation_author=JC Barrett, B Fry, J Maller, MJ Daly; citation_volume=21; citation_publication_date=2005; citation_pages=263-265; citation_doi=10.1093/bioinformatics/bth457; citation_id=CR4 citation_journal_title=Biophysical Journal; citation_title=MR diffusion tensor spectroscopy and imaging; citation_author=PJ Basser, J Mattiello, D LeBihan; citation_volume=66; citation_issue=1; citation_publication_date=1994; citation_pages=259-267; citation_doi=10.1016/S0006-3495(94)80775-1; citation_id=CR5 citation_journal_title=Genes, Brain, and Behavior; citation_title=Heritability of specific language impairment depends on diagnostic criteria; citation_author=DV Bishop, ME Hayiou-Thomas; citation_volume=7; citation_issue=3; citation_publication_date=2008; citation_pages=365-372; citation_doi=10.1111/j.1601-183X.2007.00360.x; citation_id=CR6 citation_journal_title=Neuropsychology; citation_title=Abnormal activation of temporoparietal language areas during phonetic analysis in children with dyslexia; citation_author=JI Breier, PG Simos, JM Fletcher, EM Castillo, W Zhang, AC Papanicolaou; citation_volume=17; citation_issue=4; citation_publication_date=2003; citation_pages=610-621; citation_doi=10.1037/0894-4105.17.4.610; citation_id=CR7 citation_journal_title=Cerebral Cortex; citation_title=Developmental changes in human cerebral functional organization for word generation; citation_author=TT Brown, HM Lugar, RS Coalson, FM Miezin, SE Petersen, BL Schlagger; citation_volume=15; citation_issue=3; citation_publication_date=2005; citation_pages=275-290; citation_doi=10.1093/cercor/bhh129; citation_id=CR8 citation_journal_title=Current Biology; citation_title=Neuroanatomical assessment of biological maturity; citation_author=TT Brown, JM Kuperman, Y Chung, M Erhart, C McCabe, DJ Hagler, VK Venkatraman, N Akshoomoff, DG Amaral, CS Bloss, BJ Casey, L Chang, TM Ernst, JA Frazier, JR Gruen, WE Kaufmann, T Kenet, DN Kennedy, SS Murray, ER Sowell, TL Jernigan, AM Dale; citation_volume=22; citation_issue=18; citation_publication_date=2012; citation_pages=1693-1698; citation_doi=10.1016/j.cub.2012.07.002; citation_id=CR9 citation_journal_title=Frontiers in Human Neuroscience; citation_title=Atypical right hemisphere specialization for object representations in an adolescent with specific language impairment; citation_author=TT Brown, M Erhart, D Avesar, AM Dale, E Halgren, JL Evans; citation_volume=8; citation_publication_date=2014; citation_pages=82; citation_id=CR10 citation_journal_title=Science; citation_title=Quantitative trait locus for reading disability on chromosome 6; citation_author=LR Cardon, SD Smith, DW Fulker, WJ Kimberling, BF Pennington, JC DeFries; citation_volume=266; citation_issue=5183; citation_publication_date=1994; citation_pages=276-279; citation_doi=10.1126/science.7939663; citation_id=CR11 citation_journal_title=Cerebral Cortex; citation_title=Knockdown of the dyslexia-associated gene Kiaa0319 impairs temporal responses to speech stimuli in rat primary auditory cortex; citation_author=TM Centanni, AB Booker, AM Sloan, F Chen, BJ Maher, RS Carraway, N Khodaparast, R Rennaker, JJ LoTurco, MP Kilgard; citation_volume=24; citation_issue=7; citation_publication_date=2014; citation_pages=1753-1766; citation_doi=10.1093/cercor/bht028; citation_id=CR12 citation_journal_title=Neuron; citation_title=Genetic influences on cortical regionalization in the human brain; citation_author=CH Chen, MS Panizzon, LT Eyler, TL Jernigan, W Thompson, C Fennema-Notestine, AJ Jak, MC Neale, S Hamza, MJ Lyons, MD Grant, B Fischl, LJ Seidman, MT Tsuang, WS Kremen, AM Dale; citation_volume=72; citation_issue=4; citation_publication_date=2011; citation_pages=537-544; citation_doi=10.1016/j.neuron.2011.08.021; citation_id=CR13 citation_journal_title=Science; citation_title=Hierarchical organization of human cortical surface area; citation_author=CH Chen, ED Guiterrez, W Thompson, MS Panizzon, TL Jernigan, LT Eyler, C Fennema-Notestine, AJ Jak, MC Neale, CE Franz, MJ Lyons, MD Grant, B Fischl, LJ Seidman, MT Tsuang, WS Kremen, AM Dale; citation_volume=335; citation_issue=6076; citation_publication_date=2012; citation_pages=1634-1636; citation_doi=10.1126/science.1215330; citation_id=CR14 citation_journal_title=NeuroImage; citation_title=Variants in the DYX2 locus are associated with altered brain activation on reading-related brain regions in subjects with reading disability; citation_author=N Cope, JD Eicher, H Meng, CJ Gibson, K Hager, C Lacadie, RK Fulbright, RT Constable, GP Page, JR Gruen; citation_volume=63; citation_issue=1; citation_publication_date=2012; citation_pages=148-156; citation_doi=10.1016/j.neuroimage.2012.06.037; citation_id=CR15 citation_journal_title=Biological Psychiatry; citation_title=Three dyslexia susceptibility genes, DYX1C1, DCDC2, and KIAA0319, affect temporo-parietal white matter structure; citation_author=F Darki, M Peyrard-Janvid, H Matsson, J Kere, T Klingberg; citation_volume=72; citation_issue=8; citation_publication_date=2012; citation_pages=671-676; citation_doi=10.1016/j.biopsych.2012.05.008; citation_id=CR16 citation_journal_title=Human Genetics; citation_title=Refinement of the 6p21.3 quantitative trait locus influencing dyslexia: linkage and association analysis; citation_author=KE Deffenbacher, JB Jenyon, DM Hoover, RK Olson, BF Pennington, JC DeFries, SD Smith; citation_volume=115; citation_issue=2; citation_publication_date=2004; citation_pages=128-138; citation_doi=10.1007/s00439-004-1126-6; citation_id=CR17 citation_journal_title=Behavior Genetics; citation_title=Evidence for a genetic aetiology in reading disability of twins; citation_author=JC DeFries, DW Fulker, MC LaBuda; citation_volume=17; citation_issue=3; citation_publication_date=1987; citation_pages=263-277; citation_doi=10.1007/BF01065506; citation_id=CR18 citation_journal_title=PLoS Genetics; citation_title=A common variant associated with dyslexia reduces expression of the KIAA0319 gene; citation_author=MY Dennis, S Paracchini, TS Scerri, L Prokunina-Olsson, JC Knight, R Wade-Martins, P Coggill, S Beck, ED Green, AP Monaco; citation_volume=5; citation_publication_date=2009; citation_doi=10.1371/journal.pgen.1000436; citation_id=CR19 citation_journal_title=Translational Psychiatry; citation_title=Schizophrenia-risk variant rs6994992 in the neuregulin-1 gene on brain development trajectories in typically developing children; citation_author=V Douet, L Chang, A Pritchett, K Lee, B Keating, H Bartsch, TL Jernigan, A Dale, N Akshoomoff, S Murray, C Bloss, DN Kennedy, D Amaral, J Gruen, WE Kaufmann, BJ Casey, E Sowell, T Ernst; citation_volume=4; citation_publication_date=2014; citation_doi=10.1038/tp.2014.41; citation_id=CR20 citation_journal_title=Molecular Genetics and Metabolism; citation_title=Imaging-genetics in dyslexia: connecting risk genetic variants to brain neuroimaging and ultimately to reading impairments; citation_author=JD Eicher, JR Gruen; citation_volume=110; citation_issue=3; citation_publication_date=2013; citation_pages=201-212; citation_doi=10.1016/j.ymgme.2013.07.001; citation_id=CR21 citation_journal_title=Genes, Brain, and Behavior; citation_title=Genome-wide association study of shared components of reading disability and language impairment; citation_author=JD Eicher, NR Powers, LL Miller, N Akshoomoff, DG Amaral, CS Bloss, O Libiger, NJ Schork, BF Darst, BJ Casey, L Chang, T Ernst, J Frazier, WE Kaufmann, B Keating, T Kenet, D Kennedy, S Mostofsky, SS Murray, ER Sowell, H Bartsch, JM Kuperman, TT Brown, DJ Hagler, AM Dale, TL Jernigan, B St Pourcain, G Davey Smith, SM Ring, JR Gruen; citation_volume=12; citation_issue=8; citation_publication_date=2013; citation_pages=792-801; citation_doi=10.1111/gbb.12085; citation_id=CR22 citation_journal_title=Human Genetics; citation_title=Characterization of the DYX2 locus on chromosome 6p22 with reading disability, language impairment, and IQ; citation_author=JD Eicher, NR Powers, LL Miller, KL Mueller, S Mascheretti, C Marino, EG Willcutt, JC DeFries, RK Olson, SD Smith, BF Pennington, JB Tomblin, SM Ring, JR Gruen; citation_volume=133; citation_issue=7; citation_publication_date=2014; citation_pages=869-881; citation_doi=10.1007/s00439-014-1427-3; citation_id=CR23 citation_journal_title=Journal of Medical Genetics; citation_title=A new gene (DYX3) for dyslexia is located on chromosome 2; citation_author=T Fagerheim, P Raeymaekers, FE Tønnessen, M Pedersen, L Tranebjaerg, HA Lubs; citation_volume=36; citation_issue=9; citation_publication_date=1999; citation_pages=664-669; citation_id=CR24 citation_journal_title=NeuroImage; citation_title=FreeSurfer; citation_author=B Fischl; citation_volume=62; citation_issue=2; citation_publication_date=2012; citation_pages=774-781; citation_doi=10.1016/j.neuroimage.2012.01.021; citation_id=CR25 citation_journal_title=Neuron; citation_title=Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain; citation_author=B Fischl, DH Salat, E Busa, M Albert, M Dieterich, C Haselgrove, A Kouwe, R Killiany, S Klaveness, A Montillo, N Makris, B Rosen, AM Dale; citation_volume=33; citation_issue=3; citation_publication_date=2002; citation_pages=41-55; citation_doi=10.1016/S0896-6273(02)00569-X; citation_id=CR26 citation_journal_title=Proceedings of the National Academy of Sciences of the United States of America; citation_title=Multimodal imaging of the self-regulating developing brain; citation_author=AM Fjell, KB Walhovd, TT Brown, JM Kuperman, Y Chung, DJ Hagler, V Venkatraman, JC Roddey, M Erhart, C McCabe, N Akshoomoff, DG Amaral, CS Bloss, O Libiger, BF Darst, NJ Schork, BJ Casey, L Chang, TM Ernst, JR Gruen, WE Kaufmann, T Kenet, J Frazier, SS Murray, ER Sowell, P Zijl, S Mostofsky, TL Jernigan, AM Dale; citation_volume=109; citation_issue=48; citation_publication_date=2012; citation_pages=19620-19625; citation_doi=10.1073/pnas.1208243109; citation_id=CR27 citation_journal_title=American Journal of Human Genetics; citation_title=A 77-kilobase region of chromosome 6p22.2 is associated with dyslexia in families from the United Kingdom and from the United States; citation_author=C Francks, S Paracchini, SD Smith, AJ Richardson, TS Scerri, LR Cardon, AJ Marlow, IL MacPhie, J Walter, BF Pennington, SE Fisher, RK Olson, JC DeFries, JF Stein, AP Monaco; citation_volume=75; citation_publication_date=2004; citation_pages=1046-1058; citation_doi=10.1086/426404; citation_id=CR28 citation_journal_title=American Journal of Human Genetics; citation_title=Quantitative-trait locus for specific language and reading deficits on chromosome 6p; citation_author=J Gayán, SD Smith, SS Cherny, LR Cardon, DW Fulker, AM Brower, RK Olson, BF Pennington, JC DeFries; citation_volume=64; citation_issue=1; citation_publication_date=1999; citation_pages=157-164; citation_doi=10.1086/302191; citation_id=CR29 citation_journal_title=Current Opinion in Neurobiology; citation_title=Decoding the genetics of speech and language; citation_author=SA Graham, SE Fisher; citation_volume=23; citation_issue=1; citation_publication_date=2013; citation_pages=43-51; citation_doi=10.1016/j.conb.2012.11.006; citation_id=CR30 citation_journal_title=Human Brain Mapping; citation_title=Automated white-matter tractography using a probabilistic diffusion tensor atlas: application to temporal lobe epilepsy; citation_author=DJ Hagler, ME Ahmadi, J Kuperman, D Holland, CR McDonald, E Halgren, AM Dale; citation_volume=30; citation_issue=5; citation_publication_date=2009; citation_pages=1535-1547; citation_doi=10.1002/hbm.20619; citation_id=CR31 citation_journal_title=Molecular Psychiatry; citation_title=Further evidence that the KIAA0319 gene confers susceptibility to developmental dyslexia; citation_author=D Harold, S Paracchini, T Scerri, M Dennis, N Cope, G Hill, V Moskvina, J Walter, AJ Richardson, MJ Owen, JF Stein, ED Green, MC O’Donovan, J Williams, AP Monaco; citation_volume=11; citation_issue=12; citation_publication_date=2006; citation_pages=1085-1091; citation_doi=10.1038/sj.mp.4001904; citation_id=CR32 citation_journal_title=NeuroImage; citation_title=Efficient correction of inhomogeneous static magnetic field-induced distortion in echo planar imaging; citation_author=D Holland, JM Kuperman, AM Dale; citation_volume=50; citation_issue=1; citation_publication_date=2010; citation_pages=175-183; citation_doi=10.1016/j.neuroimage.2009.11.044; citation_id=CR33 citation_journal_title=Schizophrenia Research; citation_title=Genetic influences of cortical gray matter in language-related regions in healthy controls and schizophrenia; citation_author=S Jamadar, NR Powers, SA Meda, J Gelernter, JR Gruen, GD Pearlson; citation_volume=129; citation_issue=2–3; citation_publication_date=2011; citation_pages=141-148; citation_doi=10.1016/j.schres.2011.03.027; citation_id=CR34 citation_journal_title=NeuroImage; citation_title=Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data; citation_author=J Jovicich, S Czanner, D Greve, E Haley, A Kouew, R Gollub, D Kennedy, F Schimitt, G Brown, J Macfall, B Fischl, A Dale; citation_volume=30; citation_issue=2; citation_publication_date=2006; citation_pages=436-443; citation_doi=10.1016/j.neuroimage.2005.09.046; citation_id=CR35 citation_journal_title=Journal of Medical Genetics; citation_title=A genome scan for developmental dyslexia confirms linkage to chromosome 2p11 and suggests a new locus on 7q32; citation_author=N Kaminen, K Hannula-Jouppi, M Kestilä, P Lahermo, K Muller, M Kaaranen, B Myllyluoma, A Voutilainen, H Lyytinen, J Nopola-Hemmi, J Kere; citation_volume=40; citation_issue=5; citation_publication_date=2003; citation_pages=340-345; citation_doi=10.1136/jmg.40.5.340; citation_id=CR36 citation_journal_title=American Journal of Human Genetics; citation_title=Evidence for linkage and association with reading disability on 6p21.3-22; citation_author=DE Kaplan, J Gayán, J Ahn, TW Won, D Pauls, RK Olson, JC DeFries, F Wood, BF Pennington, GP Page, SD Smith, JR Gruen; citation_volume=70; citation_issue=5; citation_publication_date=2002; citation_pages=1287-1298; citation_doi=10.1086/340449; citation_id=CR37 citation_journal_title=Human Brain Mapping; citation_title=Developmental dyslexia: gray matter abnormalities in the occipitotemporal cortex; citation_author=M Kronbichler, H Wimmer, W Staffen, F Hutzler, A Mair, G Ladurner; citation_volume=29; citation_issue=5; citation_publication_date=2008; citation_pages=613-625; citation_doi=10.1002/hbm.20425; citation_id=CR38 citation_journal_title=Brain Imaging and Behavior; citation_title=Polymorphism of DCDC2 reveals differences in cortical morphology of healthy individuals-a preliminary voxel based morphometry study; citation_author=SA Meda, J Gelernter, JR Gruen, VD Calhoun, H Meng, NA Cope, GD Pearlson; citation_volume=2; citation_issue=1; citation_publication_date=2008; citation_pages=21-26; citation_doi=10.1007/s11682-007-9012-1; citation_id=CR39 citation_journal_title=Annals of Neurology; citation_title=Multiple loci influencing hippocampal degeneration identified by genome scan; citation_author=SA Melville, J Buros, AR Parrado, B Vardarajan, MW Logue, L Shen, SL Risacher, S Kim, G Jun, C DeCarli, KL Lunetta, CT Baldwin, AJ Saykin, LA Farrer; citation_volume=72; citation_issue=1; citation_publication_date=2012; citation_pages=65-75; citation_doi=10.1002/ana.23644; citation_id=CR40 citation_journal_title=Proceedings of the National Academy of Sciences of the United States of America; citation_title=DCDC2 is associated with reading disability and modulates neuronal development in the brain; citation_author=H Meng, SD Smith, K Hager, M Held, J Liu, RK Olson, BF Pennington, JC DeFries, J Gelernter, T O’Reilly-Pol, S Somlo, P Skudlarski, SE Shaywitz, BA Shaywitz, K Marchione, Y Wang, M Paramasivam, JJ LoTurco, GP Page, JR Gruen; citation_volume=102; citation_publication_date=2005; citation_pages=17053-17058; citation_doi=10.1073/pnas.0508591102; citation_id=CR41 citation_journal_title=Genome Medicine; citation_title=Recent advances in the genetics of language impairment; citation_author=DF Newbury, SE Fisher, AP Monaco; citation_volume=2; citation_issue=1; citation_publication_date=2010; citation_pages=6; citation_doi=10.1186/gm127; citation_id=CR42 citation_journal_title=Behavior Genetics; citation_title=Investigation of dyslexia and SLI risk variants in reading- and language-impaired subjects; citation_author=DF Newbury, S Paracchini, TS Scerri, L Winchester, L Addis, AJ Richarson, J Walter, JF Stein, JB Talcott, AP Monaco; citation_volume=41; citation_issue=1; citation_publication_date=2011; citation_pages=90-104; citation_doi=10.1007/s10519-010-9424-3; citation_id=CR43 citation_journal_title=Human Molecular Genetics; citation_title=The chromosome 6p22 haplotype associated with dyslexia reduces the expression of KIAA0319, a novel gene involved in neuronal migration; citation_author=S Paracchini, A Thomas, S Castro, C Lai, M Paramasivam, Y Wang, BJ Keating, JM Taylor, DF Hacking, T Scerri, C Francks, AJ Richardson, R Wade-Martins, JF Stein, JC Knight, AJ Copp, J LoTurco, AP Monaco; citation_volume=15; citation_publication_date=2006; citation_pages=1659-1666; citation_doi=10.1093/hmg/ddl089; citation_id=CR44 citation_journal_title=Genes, Brain, and Behavior; citation_title=Analysis of dyslexia candidate genes in the Raine cohort representing the general Australian population; citation_author=S Paracchini, QW Ang, FJ Stanley, AP Monaco, CE Pennell, AJ Whitehouse; citation_volume=10; citation_issue=2; citation_publication_date=2011; citation_pages=158-165; citation_doi=10.1111/j.1601-183X.2010.00651.x; citation_id=CR45 citation_journal_title=Annual Review of Psychology; citation_title=Relations among speech, language, and reading disorders; citation_author=BF Pennington, DVM Bishop; citation_volume=60; citation_publication_date=2009; citation_pages=283-306; citation_doi=10.1146/annurev.psych.60.110707.163548; citation_id=CR46 citation_journal_title=Cerebral Cortex; citation_title=The effect of variation in expression of the candidate dyslexia susceptibility gene homolog Kiaa0319 on neuronal migration and dendritic morphology in the rat; citation_author=VJ Peschansky, TJ Burbridge, AJ Volz, C Fiondella, Z Wissner-Gross, AM Galaburda, JJ LoTurco, GD Rosen; citation_volume=20; citation_issue=4; citation_publication_date=2010; citation_pages=884-897; citation_doi=10.1093/cercor/bhp154; citation_id=CR47 citation_journal_title=Human Genetics; citation_title=Fine mapping of the 2p11 dyslexia locus and exclusion of TACr1 as a candidate gene; citation_author=M Peyrard-Janvid, H Anthoni, P Onkamo, P Lahermo, M Zucchelli, N Kaminen, K Hannula-Jouppi, J Nopola-Hemmi, A Voutilainen, H Lyytinen, J Kere; citation_volume=114; citation_issue=5; citation_publication_date=2004; citation_pages=510-516; citation_doi=10.1007/s00439-004-1103-0; citation_id=CR48 citation_journal_title=Radiology; citation_title=Diffusion tensor MR imaging of the human brain; citation_author=C Pierpaoli, P Jezzard, PJ Basser, A Barnett, G Chiro; citation_volume=201; citation_issue=3; citation_publication_date=1996; citation_pages=637-648; citation_doi=10.1148/radiology.201.3.8939209; citation_id=CR49 citation_journal_title=Journal of Neuroscience; citation_title=Genetics variants of FOXP2 and KIAA0319/TTRAP/THEM2 locus are associated with altered brain activation in distinct language-related regions; citation_author=P Pinel, F Fauchereau, A Moreno, A Barbot, M Lathrop, D Zelenika, D Bihan, JB Poline, T Bourgeron, S Dehaene; citation_volume=32; citation_issue=3; citation_publication_date=2012; citation_pages=817-825; citation_doi=10.1523/JNEUROSCI.5996-10.2012; citation_id=CR50 citation_journal_title=American Journal of Human Genetics; citation_title=Alleles of a polymorphic ETV6 binding site in DCDC2 confer risk of reading and language impairment; citation_author=NR Powers, JD Eicher, F Butter, Y Kong, LL Miller, SM Ring, M Mann, JR Gruen; citation_volume=93; citation_issue=1; citation_publication_date=2013; citation_pages=19-28; citation_doi=10.1016/j.ajhg.2013.05.008; citation_id=CR51 citation_journal_title=Biological Psychiatry; citation_title=DCDC2, KIAA0319, and CMIP are associated with reading-related traits; citation_author=TS Scerri, AP Morris, LL Buckingham, DF Newbury, LL Miller, AP Monaco, DV Bishop, S Paracchini; citation_volume=70; citation_issue=3; citation_publication_date=2011; citation_pages=237-245; citation_doi=10.1016/j.biopsych.2011.02.005; citation_id=CR52 citation_journal_title=PLoS One; citation_title=The dyslexia candidate locus on 2p12 is associated with general cognitive ability and white matter structure; citation_author=TS Scerri, F Darki, DF Newbury, AJ Whitehouse, M Peyrard-Janvid, H Matsson, QW Ang, CE Pennell, S Ring, J Stein, AP Morris, AP Monaco, J Kere, JB Talcott, T Kingberg, S Paracchini; citation_volume=7; citation_issue=11; citation_publication_date=2012; citation_doi=10.1371/journal.pone.0050321; citation_id=CR53 citation_journal_title=American Journal of Human Genetics; citation_title=Strong genetic evidence of DCDC2 as a susceptibility gene for dyslexia; citation_author=J Schumacher, H Anthoni, F Dahdouh, IR König, AM Hillmer, N Kluck, M Manthey, E Plume, A Warnke, H Remschmidt, J Hülsmann, S Cichon, CM Lindgren, P Propping, M Zucchelli, A Ziegler, M Peyrard-Janvid, G Schulte-Körne, MM Nöthen, J Kere; citation_volume=78; citation_issue=1; citation_publication_date=2006; citation_pages=52-62; citation_doi=10.1086/498992; citation_id=CR54 citation_journal_title=Proceedings of the National Academy of Sciences of the United States of America; citation_title=Functional disruption in the organization of the brain for reading in dyslexia; citation_author=SE Shaywitz, BA Shaywitz, KR Pugh, RK Fulbright, RT Constable, WE Mencl, DP Shankweiler, AM Liberman, P Skudlarski, JM Fletcher, L Katz, KE Marchione, C Lacadie, C Gatenby, JC Gore; citation_volume=95; citation_issue=5; citation_publication_date=1998; citation_pages=2636-2641; citation_doi=10.1073/pnas.95.5.2636; citation_id=CR55 citation_journal_title=Journal of Child Psychology and Psychiatry; citation_title=Linkage of speech sound disorder to reading disability loci; citation_author=SD Smith, BF Pennington, R Boada, LD Shriberg; citation_volume=46; citation_issue=1; citation_publication_date=2005; citation_pages=1057-1066; citation_doi=10.1111/j.1469-7610.2005.01534.x; citation_id=CR56 citation_journal_title=International Journal of Developmental Neuroscience; citation_title=Neocortical disruption and behavioral impairments in rats following in utero RNAi of candidate dyslexia risk gene Kiaa0319; citation_author=CE Szalkowski, CG Fiondella, AM Galaburda, GD Rosen, JJ Loturco, RH Fitch; citation_volume=30; citation_issue=4; citation_publication_date=2012; citation_pages=293-302; citation_doi=10.1016/j.ijdevneu.2012.01.009; citation_id=CR57 citation_journal_title=International Journal of Developmental Neuroscience; citation_title=The effects of Kiaa0319 knockdown on cortical and subcortical anatomy in male rats; citation_author=CE Szalkowski, CF Fiondella, DT Truong, GD Rosen, JJ LoTurco, RH Fitch; citation_volume=31; citation_issue=2; citation_publication_date=2013; citation_pages=116-122; citation_doi=10.1016/j.ijdevneu.2012.11.008; citation_id=CR58 citation_journal_title=Neuroreport; citation_title=Disrupted neural responses to phonological and orthographic processing in dyslexic children: an fMRI study; citation_author=E Temple, RA Poldrack, J Salidis, GK Deutsch, P Tallal, MM Merzenich, JD Gabrieli; citation_volume=12; citation_issue=2; citation_publication_date=2001; citation_pages=299-307; citation_doi=10.1097/00001756-200102120-00024; citation_id=CR59 citation_journal_title=Current Opinion in Neurology; citation_title=Imaging genomics; citation_author=PM Thompson, NG Martin, MJ Wright; citation_volume=23; citation_issue=4; citation_publication_date=2010; citation_pages=368-373; citation_id=CR60 citation_journal_title=Twin Research and Human Genetics; citation_title=Heritability of verbal and performance intelligence in a pediatric longitudinal sample; citation_author=IL Soelen, RM Brouwer, M Leeuwen, RS Kahn, HE Hulshoff Pol, DI Boomsma; citation_volume=14; citation_issue=2; citation_publication_date=2011; citation_pages=119-128; citation_doi=10.1375/twin.14.2.119; citation_id=CR61 citation_journal_title=Proceedings of the National Academy of Sciences of the United States of America; citation_title=Long-term influence of normal variation in neonatal characteristics on human brain development; citation_author=KB Walhovd, AM Fjell, TT Brown, JM Kuperman, Y Chung, DJ Hagler, JC Roddey, M Erhart, C McCabe, N Akshoomoff, DG Amaral, CS Bloss, O Libiger, NJ Schork, BF Darst, BJ Casey, L Chang, TM Ernst, J Frazier, JR Gruen, WE Kaufmann, SS Murray, P Zijl, S Mostofsky, AM Dale; citation_volume=109; citation_issue=49; citation_publication_date=2012; citation_pages=20089-20094; citation_doi=10.1073/pnas.1208180109; citation_id=CR62 citation_journal_title=Medical Image Analysis; citation_title=Multi-modal volume registration by maximization of mutual information; citation_author=WM Wells, P Viola, H Atsumi, S Nakajima, R Kikinis; citation_volume=1; citation_issue=1; citation_publication_date=1996; citation_pages=35-51; citation_doi=10.1016/S1361-8415(01)80004-9; citation_id=CR63 citation_journal_title=Journal of Magnetic Resonance Imaging; citation_title=Correction of eddy-current distortions in diffusion tensor images using the known directions and strengths of diffusion gradients; citation_author=J Zhuang, J Hrabe, A Kangarlu, D Xu, R Bansal, CA Branch, BS Peterson; citation_volume=24; citation_issue=5; citation_publication_date=2006; citation_pages=1188-1193; citation_doi=10.1002/jmri.20727; citation_id=CR64