Diffusion tensor imaging in first degree relatives of schizophrenia and bipolar disorder patients

Schizophrenia Research

Volumn 161, Issue 2-3, 2015, Pages 329-339

  Arat, Hidayet E ^a,b   Chouinard, Virginie Anne ^b,c   Cohen, Bruce M ^b,c   Lewandowski, Kathryn E ^b,c   Öngür, Dost ^b,c  

^a DOKUZ EYLUL UNIVERSITY   (Turkey)

^b MCLEAN HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

At risk; DTI; Endophenotype; Psychosis; White matter

Indexed keywords

ANGULAR GYRUS; ANTERIOR CINGULATE; BIPOLAR DISORDER; CAPSULA INTERNA; COMPARATIVE STUDY; CORPUS CALLOSUM; DIFFUSION COEFFICIENT; DIFFUSION TENSOR IMAGING; FIRST DEGREE RELATIVE; FRACTIONAL ANISOTROPY; FRONTAL GYRUS; HIPPOCAMPUS; HUMAN; OCCIPITAL LOBE; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PHYSICAL PARAMETERS; POSTERIOR CINGULATE; PREFRONTAL CORTEX; RADIAL DIFFUSIVITY; REVIEW; SCHIZOPHRENIA; TEMPORAL LOBE; WHITE MATTER; BRAIN; ENDOPHENOTYPE; FAMILY; PATHOLOGY;

BIPOLAR DISORDER; BRAIN; DIFFUSION TENSOR IMAGING; ENDOPHENOTYPES; FAMILY; HUMANS; SCHIZOPHRENIA; WHITE MATTER;

EID: 84921548226     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2014.12.008     Document Type: Review

References (88)

1. Altshuler L.L., Curran J.G., Hauser P., Mintz J., Denicoff K., Post R. T2 hyperintensities in bipolar disorder: magnetic resonance imaging comparison and literature meta-analysis. Am. J. Psychiatry 1995, 152:1139-1144.
2. Aydin K., Ucok A., Guler J. Altered metabolic integrity of corpus callosum among individuals at ultra high risk of schizophrenia and first-episode patients. Biol. Psychiatry 2008, 64:750-757. 10.1016/j.biopsych.2008.04.007.
3. Badner J.A., Gershon E.S. Meta-analysis of whole-genome linkage scans of bipolar disorder and schizophrenia. Mol. Psychiatry 2002, 7:405-411. 10.1038/sj.mp.4001012.
4. Balanzá-Martínez V., Rubio C., Selva-Vera G., Martinez-Aran A., Sánchez-Moreno J., Salazar-Fraile J., Vieta E., Tabarés-Seisdedos R. Neurocognitive endophenotypes (endophenocognitypes) from studies of relatives of bipolar disorder subjects: a systematic review. Neurosci. Biobehav. Rev. 2008, 32:1426-1438. 10.1016/j.neubiorev.2008.05.019.
5. Bertisch H., Li D., Hoptman M.J., Delisi L.E. Heritability estimates for cognitive factors and brain white matter integrity as markers of schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2010, 153B:885-894. 10.1002/ajmg.b.31054.
6. Beyer J.L., Young R., Kuchibhatla M., Krishnan K.R.R. Hyperintense MRI lesions in bipolar disorder: a meta-analysis and review. Int. Rev. Psychiatry 2009, 21:394-409. 10.1080/09540260902962198.
7. Boos H.B.M., Mandl R.C.W., van Haren N.E.M., Cahn W., van Baal G.C.M., Kahn R.S., Hulshoff Pol H.E. Tract-based diffusion tensor imaging in patients with schizophrenia and their non-psychotic siblings. Eur. Neuropsychopharmacol. 2013, 23:295-304. 10.1016/j.euroneuro.2012.05.015.
8. Bora E., Fornito A., Radua J., Walterfang M., Seal M., Wood S.J., Yücel M., Velakoulis D., Pantelis C. Neuroanatomical abnormalities in schizophrenia: a multimodal voxelwise meta-analysis and meta-regression analysis. Schizophr. Res. 2011, 127:46-57. 10.1016/j.schres.2010.12.020.
9. Bora E., Yucel M., Pantelis C. Cognitive endophenotypes of bipolar disorder: a meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives. J. Affect. Disord. 2009, 113:1-20. 10.1016/j.jad.2008.06.009.
10. Braff D.L., Freedman R., Schork N.J., Gottesman I.I. Deconstructing schizophrenia: an overview of the use of endophenotypes in order to understand a complex disorder. Schizophr. Bull. 2007, 33:21-32. 10.1093/schbul/sbl049.
11. Camchong J., Lim K.O., Sponheim S.R., Macdonald A.W. Frontal white matter integrity as an endophenotype for schizophrenia: diffusion tensor imaging in monozygotic twins and patients' nonpsychotic relatives. Front. Hum. Neurosci. 2009, 3:35. 10.3389/neuro.09.035.2009.
12. Carletti F., Woolley J.B., Bhattacharyya S., Perez-Iglesias R., Fusar Poli P., Valmaggia L., Broome M.R., Bramon E., Johns L., Giampietro V., Williams S.C.R., Barker G.J., McGuire P.K. Alterations in white matter evident before the onset of psychosis. Schizophr. Bull. 2012, 38:1170-1179. 10.1093/schbul/sbs053.
13. Chaddock C.A., Barker G.J., Marshall N., Schulze K., Hall M.H., Fern A., Walshe M., Bramon E., Chitnis X.A., Murray R., McDonald C. White matter microstructural impairments and genetic liability to familial bipolar I disorder. Br. J. Psychiatry 2009, 194:527-534. 10.1192/bjp.bp.107.047498.
14. Clark K.A., Nuechterlein K.H., Asarnow R.F., Hamilton L.S., Phillips O.R., Hageman N.S., Woods R.P., Alger J.R., Toga A.W., Narr K.L. Mean diffusivity and fractional anisotropy as indicators of disease and genetic liability to schizophrenia. J. Psychiatr. Res. 2011, 45:980-988. 10.1016/j.jpsychires.2011.01.006.
15. Contet C., Le D., Roberts A.J., Steven N., Koob G.F. Poster session III. Neuropsychopharmacology 2011, 36:S324-S449. 10.1038/npp.2011.293.
16. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215. 10.1038/nrn755.
17. DeLisi L.E., Szulc K.U., Bertisch H., Majcher M., Brown K., Bappal A., Branch C.A., Ardekani B.A. Early detection of schizophrenia by diffusion weighted imaging. Psychiatry Res. 2006, 148:61-66. 10.1016/j.pscychresns.2006.04.010.
18. Domen P.A.E., Michielse S., Gronenschild E., Habets P., Roebroeck A., Schruers K., van Os J., Marcelis M. Microstructural white matter alterations in psychotic disorder: a family-based diffusion tensor imaging study. Schizophr. Res. 2013, 146:291-300. 10.1016/j.schres.2013.03.002.
19. Duncan L.E., Holmans P.A., Lee P.H., O'Dushlaine C.T., Kirby A.W., Smoller J.W., Öngür D., Cohen B.M. Pathway analyses implicate glial cells in schizophrenia. PLoS ONE 2014, 9:e89441. 10.1371/journal.pone.0089441.
20. Ellison-Wright I., Bullmore E. Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr. Res. 2009, 108:3-10. 10.1016/j.schres.2008.11.021.
21. Emsell L., Chaddock C., Forde N., Van Hecke W., Barker G.J., Leemans A., Sunaert S., Walshe M., Bramon E., Cannon D., Murray R., McDonald C. White matter microstructural abnormalities in families multiply affected with bipolar I disorder: a diffusion tensor tractography study. Psychol. Med. 2013, 1-12. 10.1017/S0033291713002845.
22. Forstmann B.U., Jahfari S., Scholte H.S., Wolfensteller U., van den Wildenberg W.P.M., Ridderinkhof K.R. Function and structure of the right inferior frontal cortex predict individual differences in response inhibition: a model-based approach. J. Neurosci. 2008, 28:9790-9796. 10.1523/JNEUROSCI. 1465-08.2008.
23. Francis A.N., Bhojraj T.S., Prasad K.M., Kulkarni S., Montrose D.M., Eack S.M., Keshavan M.S. Abnormalities of the corpus callosum in non-psychotic high-risk offspring of schizophrenia patients. Psychiatry Res. 2011, 191:9-15. 10.1016/j.pscychresns.2010.09.007.
24. Francis A.N., Seidman L.J., Jabbar G.A., Mesholam-Gately R., Thermenos H.W., Juelich R., Proal A.C., Shenton M., Kubicki M., Mathew I., Keshavan M., Delisi L.E. Alterations in brain structures underlying language function in young adults at high familial risk for schizophrenia. Schizophr. Res. 2012, 141:65-71. 10.1016/j.schres.2012.07.015.
25. Frazier J.A., Breeze J.L., Papadimitriou G., Kennedy D.N., Hodge S.M., Moore C.M., Howard J.D., Rohan M.P., Caviness V.S., Makris N. White matter abnormalities in children with and at risk for bipolar disorder. Bipolar Disord. 2007, 9:799-809. 10.1111/j.1399-5618.2007.00482.x.
26. Glahn D.C., Almasy L., Barguil M., Hare E., Peralta J.M., Kent J.W., Dassori A., Contreras J., Pacheco A., Lanzagorta N., Nicolini H., Raventós H., Escamilla M.A. Neurocognitive endophenotypes for bipolar disorder identified in multiplex multigenerational families. Arch. Gen. Psychiatry 2010, 67:168-177. 10.1001/archgenpsychiatry.2009.184.
27. Goghari V.M., Billiet T., Sunaert S., Emsell L. A diffusion tensor imaging family study of the fornix in schizophrenia. Schizophr. Res. 2014, 10.1016/j.schres.2014.09.037.
28. Gottesman I.I., Gould T.D. Reviews and Overviews. The Endophenotype Concept in Psychiatry: Etymology and Strategic Intentions 2003, 636-645.
29. Green E.K., Raybould R., Macgregor S., Gordon-Smith K., Heron J., Hyde S., Grozeva D., Hamshere M., Williams N., Owen M.J., O'Donovan M.C., Jones L., Jones I., Kirov G., Craddock N. Operation of the schizophrenia susceptibility gene, neuregulin 1, across traditional diagnostic boundaries to increase risk for bipolar disorder. Arch. Gen. Psychiatry 2005, 62:642-648. 10.1001/archpsyc.62.6.642.
30. Green M.J., Cahill C.M., Malhi G.S. The cognitive and neurophysiological basis of emotion dysregulation in bipolar disorder. J. Affect. Disord. 2007, 103:29-42. 10.1016/j.jad.2007.01.024.
31. Hajek T., Carrey N., Alda M. Neuroanatomical abnormalities as risk factors for bipolar disorder. Bipolar Disord. 2005, 7:393-403. 10.1111/j.1399-5618.2005.00238.x.
32. Hao Y., Yan Q., Liu H., Xu L., Xue Z., Song X., Kaneko Y., Jiang T., Liu Z., Shan B. Schizophrenia patients and their healthy siblings share disruption of white matter integrity in the left prefrontal cortex and the hippocampus but not the anterior cingulate cortex. Schizophr. Res. 2009, 114:128-135. 10.1016/j.schres.2009.07.001.
33. Hasan K.M. Diffusion tensor eigenvalues or both mean diffusivity and fractional anisotropy are required in quantitative clinical diffusion tensor MR reports: fractional anisotropy alone is not sufficient. Radiology 2006, 239:611-612. (author reply 612-3). 10.1148/radiol.2392051172.
34. Hasler G., Drevets W.C., Gould T.D., Gottesman I.I., Manji H.K. Toward constructing an endophenotype strategy for bipolar disorders. Biol. Psychiatry 2006, 60:93-105. 10.1016/j.biopsych.2005.11.006.
35. Hoptman M.J., Nierenberg J., Bertisch H.C., Catalano D., Ardekani B.A., Branch C.A., Delisi L.E. A DTI study of white matter microstructure in individuals at high genetic risk for schizophrenia. Schizophr. Res. 2008, 106:115-124. 10.1016/j.schres.2008.07.023.
36. Jacobson S., Kelleher I., Harley M., Murtagh A., Clarke M., Blanchard M., Connolly C., O'Hanlon E., Garavan H., Cannon M. Structural and functional brain correlates of subclinical psychotic symptoms in 11-13year old schoolchildren. Neuroimage 2010, 49:1875-1885. 10.1016/j.neuroimage.2009.09.015.
37. Kang Z., Wei Q., Tang Y., Li L., Zheng L., Guo X., Zhang J., Zhao J. Diffusion tensor imaging analyses of white matter in healthy siblings of schizophrenics. Zhonghua Yi Xue Za Zhi 2012, 92:2772-2774.
38. Karlsgodt K.H., Niendam T.A., Bearden C.E., Cannon T.D. White matter integrity and prediction of social and role functioning in subjects at ultra-high risk for psychosis. Biol. Psychiatry 2009, 66:562-569. 10.1016/j.biopsych.2009.03.013.
39. Karlsgodt K.H., van Erp T.G.M., Poldrack R.A., Bearden C.E., Nuechterlein K.H., Cannon T.D. Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biol. Psychiatry 2008, 63:512-518. 10.1016/j.biopsych.2007.06.017.
40. Keshavan M.S., Morris D.W., Sweeney J.A., Pearlson G., Thaker G., Seidman L.J., Eack S.M., Tamminga C. A dimensional approach to the psychosis spectrum between bipolar disorder and schizophrenia: the Schizo-Bipolar Scale. Schizophr. Res. 2011, 133:250-254. 10.1016/j.schres.2011.09.005.
41. Knöchel C., O'Dwyer L., Alves G., Reinke B., Magerkurth J., Rotarska-Jagiela A., Prvulovic D., Hampel H., Linden D.E.J., Oertel-Knöchel V. Association between white matter fiber integrity and subclinical psychotic symptoms in schizophrenia patients and unaffected relatives. Schizophr. Res. 2012, 140:129-135. 10.1016/j.schres.2012.06.001.
42. Knöchel C., Oertel-Knöchel V., Schönmeyer R., Rotarska-Jagiela A., van de Ven V., Prvulovic D., Haenschel C., Uhlhaas P., Pantel J., Hampel H., Linden D.E.J. Interhemispheric hypoconnectivity in schizophrenia: fiber integrity and volume differences of the corpus callosum in patients and unaffected relatives. Neuroimage 2012, 59:926-934. 10.1016/j.neuroimage.2011.07.088.
43. Kraepelin E. Manifestation of insanity. Z. Gesamte. Neurol. Psychiatr. 1920, 62:1-29.
44. Kumra S., Ashtari M., Cervellione K.L., Henderson I., Kester H., Roofeh D., Wu J., Clarke T., Thaden E., Kane J.M., Rhinewine J., Lencz T., Diamond A., Ardekani B.A., Szeszko P.R. White matter abnormalities in early-onset schizophrenia: a voxel-based diffusion tensor imaging study. J. Am. Acad. Child Adolesc. Psychiatry 2005, 44:934-941. 10.1097/01.chi.0000170553.15798.94.
45. Li X., Branch C.A., Bertisch H.C., Brown K., Szulc K.U., Ardekani B.A., DeLisi L.E. An fMRI study of language processing in people at high genetic risk for schizophrenia. Schizophr. Res. 2007, 91:62-72. 10.1016/j.schres.2006.12.016.
46. Linke J., King A.V., Poupon C., Hennerici M.G., Gass A., Wessa M. Impaired anatomical connectivity and related executive functions: differentiating vulnerability and disease marker in bipolar disorder. Biol. Psychiatry 2013, 74:908-916. 10.1016/j.biopsych.2013.04.010.
47. Mahon K., Burdick K.E., Ikuta T., Braga R.J., Gruner P., Malhotra A.K., Szeszko P.R. Abnormal temporal lobe white matter as a biomarker for genetic risk of bipolar disorder. Biol. Psychiatry 2013, 73:177-182. 10.1016/j.biopsych.2012.07.033.
48. McDonald C., Bullmore E.T., Sham P.C., Chitnis X., Wickham H., Bramon E., Murray R.M. Association of genetic risks for schizophrenia and bipolar disorder with specific and generic brain structural endophenotypes. Arch. Gen. Psychiatry 2004, 61:974-984. 10.1001/archpsyc.61.10.974.
49. McDonald C., Bullmore E., Sham P., Chitnis X., Suckling J., MacCabe J., Walshe M., Murray R.M. Regional volume deviations of brain structure in schizophrenia and psychotic bipolar disorder: computational morphometry study. Br. J. Psychiatry 2005, 186:369-377. 10.1192/bjp.186.5.369.
50. McIntosh A.M., Job D.E., Moorhead T.W.J., Harrison L.K., Forrester K., Lawrie S.M., Johnstone E.C. Voxel-based morphometry of patients with schizophrenia or bipolar disorder and their unaffected relatives. Biol. Psychiatry 2004, 56:544-552. 10.1016/j.biopsych.2004.07.020.
51. McIntosh A.M., Job D.E., Moorhead T.W.J., Harrison L.K., Lawrie S.M., Johnstone E.C. White matter density in patients with schizophrenia, bipolar disorder and their unaffected relatives. Biol. Psychiatry 2005, 58:254-257. 10.1016/j.biopsych.2005.03.044.
52. McIntosh A.M., Moorhead T.W.J., Job D., Lymer G.K.S., Muñoz Maniega S., McKirdy J., Sussmann J.E.D., Baig B.J., Bastin M.E., Porteous D., Evans K.L., Johnstone E.C., Lawrie S.M., Hall J. The effects of a neuregulin 1 variant on white matter density and integrity. Mol. Psychiatry 2008, 13:1054-1059. 10.1038/sj.mp.4002103.
53. McIntosh A.M., Muñoz Maniega S., Lymer G.K.S., McKirdy J., Hall J., Sussmann J.E.D., Bastin M.E., Clayden J.D., Johnstone E.C., Lawrie S.M. White matter tractography in bipolar disorder and schizophrenia. Biol. Psychiatry 2008, 64:1088-1092. 10.1016/j.biopsych.2008.07.026.
54. Mei L., Nave K.-A. Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases. Neuron 2014, 83:27-49. 10.1016/j.neuron.2014.06.007.
55. Munafò M.R., Thiselton D.L., Clark T.G., Flint J. Association of the NRG1 gene and schizophrenia: a meta-analysis. Mol. Psychiatry 2006, 11:539-546. 10.1038/sj.mp.4001817.
56. Muñoz Maniega S., Lymer G.K.S., Bastin M.E., Marjoram D., Job D.E., Moorhead T.W.J., Owens D.G., Johnstone E.C., McIntosh A.M., Lawrie S.M. A diffusion tensor MRI study of white matter integrity in subjects at high genetic risk of schizophrenia. Schizophr. Res. 2008, 106:132-139. 10.1016/j.schres.2008.09.016.
57. Narr K.L., Hageman N., Woods R.P., Hamilton L.S., Clark K., Phillips O., Shattuck D.W., Asarnow R.F., Toga A.W., Nuechterlein K.H. Mean diffusivity: a biomarker for CSF-related disease and genetic liability effects in schizophrenia. Psychiatry Res. 2009, 171:20-32. 10.1016/j.pscychresns.2008.03.008.
58. Nave K.-A. Myelination and support of axonal integrity by glia. Nature 2010, 468:244-252. 10.1038/nature09614.
59. Oertel-Knöchel V., Knöchel C., Matura S., Prvulovic D., Linden D.E.J., van de Ven V. Reduced functional connectivity and asymmetry of the planum temporale in patients with schizophrenia and first-degree relatives. Schizophr. Res. 2013, 147:331-338. 10.1016/j.schres.2013.04.024.
60. Peters B.D., de Haan L., Dekker N., Blaas J., Becker H.E., Dingemans P.M., Akkerman E.M., Majoie C.B., van Amelsvoort T., den Heeten G.J., Linszen D.H. White matter fibertracking in first-episode schizophrenia, schizoaffective patients and subjects at ultra-high risk of psychosis. Neuropsychobiology 2008, 58:19-28. 10.1159/000154476.
61. Pettersson-Yeo W., Benetti S., Marquand A.F., Dell'acqua F., Williams S.C.R., Allen P., Prata D., McGuire P., Mechelli A. Using genetic, cognitive and multi-modal neuroimaging data to identify ultra-high-risk and first-episode psychosis at the individual level. Psychol. Med. 2013, 43:2547-2562. 10.1017/S003329171300024X.
62. Phillips M.L., Drevets W.C., Rauch S.L., Lane R. Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol. Psychiatry 2003, 54:504-514. 10.1016/S0006-3223(03)00168-9.
63. Phillips M.L., Drevets W.C., Rauch S.L., Lane R. Neurobiology of emotion perception II: implications for major psychiatric disorders. Biol. Psychiatry 2003, 54:515-528. 10.1016/S0006-3223(03)00171-9.
64. Phillips M.L., Ladouceur C.D., Drevets W.C. A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol. Psychiatry 2008, 13(829):833-857. 10.1038/mp.2008.65.
65. Phillips O.R., Nuechterlein K.H., Asarnow R.F., Clark K.A., Cabeen R., Yang Y., Woods R.P., Toga A.W., Narr K.L. Mapping corticocortical structural integrity in schizophrenia and effects of genetic liability. Biol. Psychiatry 2011, 70:680-689. 10.1016/j.biopsych.2011.03.039.
66. Potash J.B. Carving chaos: genetics and the classification of mood and psychotic syndromes. Harv. Rev. Psychiatry 2006, 14:47-63. 10.1080/10673220600655780.
67. Prasad K.M., Upton C.H., Schirda C.S., Nimgaonkar V.L., Keshavan M.S. White matter diffusivity and microarchitecture among schizophrenia subjects and first-degree relatives. Schizophr. Res. 2014, 10.1016/j.schres.2014.09.045.
68. Prata D.P., Breen G., Osborne S., Munro J., St Clair D., Collier D.A. An association study of the neuregulin 1 gene, bipolar affective disorder and psychosis. Psychiatr. Genet. 2009, 19:113-116. 10.1097/YPG.0b013e32832a4f69.
69. Schretlen D.J., Cascella N.G., Meyer S.M., Kingery L.R., Testa S.M., Munro C.A., Pulver A.E., Rivkin P., Rao V.A., Diaz-Asper C.M., Dickerson F.B., Yolken R.H., Pearlson G.D. Neuropsychological functioning in bipolar disorder and schizophrenia. Biol. Psychiatry 2007, 62:179-186. 10.1016/j.biopsych.2006.09.025.
70. Shizukuishi T., Abe O., Aoki S. Diffusion tensor imaging analysis for psychiatric disorders. Magn. Reson. Med. Sci. 2013, 12:153-159.
71. Skudlarski P., Schretlen D.J., Thaker G.K., Stevens M.C., Keshavan M.S., Sweeney J.A., Tamminga C.A., Clementz B.A., O'Neil K., Pearlson G.D. Diffusion tensor imaging white matter endophenotypes in patients with schizophrenia or psychotic bipolar disorder and their relatives. Am. J. Psychiatry 2013, 170:886-898. 10.1176/appi.ajp.2013.12111448.
72. Snitz B.E., Macdonald A.W., Carter C.S. Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: a meta-analytic review of putative endophenotypes. Schizophr. Bull. 2006, 32:179-194. 10.1093/schbul/sbi048.
73. Sprooten E., Sussmann J.E., Clugston A., Peel A., McKirdy J., Moorhead T.W.J., Anderson S., Shand A.J., Giles S., Bastin M.E., Hall J., Johnstone E.C., Lawrie S.M., McIntosh A.M. White matter integrity in individuals at high genetic risk of bipolar disorder. Biol. Psychiatry 2011, 70:350-356. 10.1016/j.biopsych.2011.01.021.
74. Sprooten E., Brumbaugh M.S., Knowles E.E.M., Mckay D.R., Lewis J., Barrett J., Landau S., Cyr L., Kochunov P., Winkler A.M., Pearlson G.D., Glahn D.C. For Bipolar Disorder 2013, 1317-1325.
75. Stefansson H., Sigurdsson E., Steinthorsdottir V., Bjornsdottir S., Sigmundsson T., Ghosh S., Brynjolfsson J., Gunnarsdottir S., Ivarsson O., Chou T.T., Hjaltason O., Birgisdottir B., Jonsson H., Gudnadottir V.G., Gudmundsdottir E., Bjornsson A., Ingvarsson B., Ingason A., Sigfusson S., Hardardottir H., Harvey R.P., Lai D., Zhou M., Brunner D., Mutel V., Gonzalo A., Lemke G., Sainz J., Johannesson G., Andresson T., Gudbjartsson D., Manolescu A., Frigge M.L., Gurney M.E., Kong A., Gulcher J.R., Petursson H., Stefansson K. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 2002, 71:877-892. 10.1086/342734.
76. Szeszko P.R., Ardekani B.A., Ashtari M., Kumra S., Robinson D.G., Sevy S., Gunduz-Bruce H., Malhotra A.K., Kane J.M., Bilder R.M., Lim K.O. White matter abnormalities in first-episode schizophrenia or schizoaffective disorder: a diffusion tensor imaging study. Am. J. Psychiatry 2005, 162:602-605. 10.1176/appi.ajp.162.3.602.
77. Szeszko P.R., Robinson D.G., Ashtari M., Vogel J., Betensky J., Sevy S., Ardekani B.A., Lencz T., Malhotra A.K., McCormack J., Miller R., Lim K.O., Gunduz-Bruce H., Kane J.M., Bilder R.M. Clinical and neuropsychological correlates of white matter abnormalities in recent onset schizophrenia. Neuropsychopharmacology 2008, 33:976-984. 10.1038/sj.npp.1301480.
78. Thomason M.E., Thompson P.M. Diffusion imaging, white matter, and psychopathology. Annu. Rev. Clin. Psychol. 2011, 7:63-85. 10.1146/annurev-clinpsy-032210-104507.
79. Umarova R.M., Saur D., Schnell S., Kaller C.P., Vry M.-S., Glauche V., Rijntjes M., Hennig J., Kiselev V., Weiller C. Structural connectivity for visuospatial attention: significance of ventral pathways. Cereb. Cortex 2010, 20:121-129. 10.1093/cercor/bhp086.
80. Van der Schot A.C., Vonk R., Brans R.G.H., van Haren N.E.M., Koolschijn P.C.M.P., Nuboer V., Schnack H.G., van Baal G.C.M., Boomsma D.I., Nolen W.A., Hulshoff Pol H.E., Kahn R.S. Influence of genes and environment on brain volumes in twin pairs concordant and discordant for bipolar disorder. Arch. Gen. Psychiatry 2009, 66:142-151. 10.1001/archgenpsychiatry.2008.541.
81. Vederine F.-E., Wessa M., Leboyer M., Houenou J. A meta-analysis of whole-brain diffusion tensor imaging studies in bipolar disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 2011, 35:1820-1826. 10.1016/j.pnpbp.2011.05.009.
82. Versace A., Ladouceur C.D., Romero S., Birmaher B., Axelson D.A., Kupfer D.J., Phillips M.L. Altered development of white matter in youth at high familial risk for bipolar disorder: a diffusion tensor imaging study. J. Am. Acad. Child Adolesc. Psychiatry 2010, 49:1249-1259. (1259.e1.). 10.1016/j.jaac.2010.09.007.
83. Von Hohenberg C.C., Pasternak O., Kubicki M., Ballinger T., Vu M.-A., Swisher T., Green K., Giwerc M., Dahlben B., Goldstein J.M., Woo T.-U.W., Petryshen T.L., Mesholam-Gately R.I., Woodberry, K.a, Thermenos H.W., Mulert C., McCarley R.W., Seidman L.J., Shenton M.E. White matter microstructure in individuals at clinical high risk of psychosis: a whole-brain diffusion tensor imaging study. Schizophr. Bull. 2014, 40:895-903. 10.1093/schbul/sbt079.
84. Wang F., Jiang T., Sun Z., Teng S.-L., Luo X., Zhu Z., Zang Y., Zhang H., Yue W., Qu M., Lu T., Hong N., Huang H., Blumberg H.P., Zhang D. Neuregulin 1 genetic variation and anterior cingulum integrity in patients with schizophrenia and healthy controls. J. Psychiatry Neurosci. 2009, 34:181-186.
85. Wang Q., Deng W., Huang C., Li M., Ma X., Wang Y., Jiang L., Lui S., Huang X., Chua S.E., Cheung C., McAlonan G.M., Sham P.C., Murray R.M., Collier D.A., Gong Q., Li T. Abnormalities in connectivity of white-matter tracts in patients with familial and non-familial schizophrenia. Psychol. Med. 2011, 41:1691-1700. 10.1017/S0033291710002412.
86. White T., Kendi A.T.K., Lehéricy S., Kendi M., Karatekin C., Guimaraes A., Davenport N., Schulz S.C., Lim K.O. Disruption of hippocampal connectivity in children and adolescents with schizophrenia-a voxel-based diffusion tensor imaging study. Schizophr. Res. 2007, 90:302-307. 10.1016/j.schres.2006.09.032.
87. Winterer G., Konrad A., Vucurevic G., Musso F., Stoeter P., Dahmen N. Association of 5' end neuregulin-1 (NRG1) gene variation with subcortical medial frontal microstructure in humans. Neuroimage 2008, 40:712-718. 10.1016/j.neuroimage.2007.12.041.
88. Zuliani R., Moorhead T.W.J., Bastin M.E., Johnstone E.C., Lawrie S.M., Brambilla P., O'Donovan M.C., Owen M.J., Hall J., McIntosh A.M. Genetic variants in the ErbB4 gene are associated with white matter integrity. Psychiatry Res. 2011, 191:133-137. 10.1016/j.pscychresns.2010.11.001.