Less efficient information transfer in cys-allele carriers of DISC1: A brain network study based on diffusion MRI

Cerebral Cortex

Volumn 23, Issue 7, 2013, Pages 1715-1723

  Li, Yonghui ^a,b   Liu, Bing ^a   Hou, Bing ^a   Qin, Wen ^c   Wang, Dawei ^c   Yu, Chunshui ^c   Jiang, Tianzi ^a,b,d  

^a INSTITUTE OF AUTOMATION   (China)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

fiber tractography; gene; neuroimaging; schizophrenia; white matter

Indexed keywords

DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN;

ADULT; ARTICLE; DIFFUSION WEIGHTED IMAGING; FEMALE; FUNCTIONAL NEUROIMAGING; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HOMOZYGOTE; HUMAN; MALE; NERVE CELL NETWORK; NORMAL HUMAN; PRIORITY JOURNAL; SCHIZOPHRENIA; TRACTOGRAPHY; WHITE MATTER;

FIBER TRACTOGRAPHY; GENE; NEUROIMAGING; SCHIZOPHRENIA; WHITE MATTER;

ADOLESCENT; ADULT; ALLELES; BRAIN; DIFFUSION TENSOR IMAGING; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MALE; NERVE TISSUE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84878889913     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs167     Document Type: Article

References (61)

1. Achard S, Bullmore E. 2007. Efficiency and cost of economical brain functional networks. PLoS Comput Biol. 3:e17.
2. Ashburner J, Friston KJ. 2000. Voxel-based morphometry-the methods. Neuroimage. 11:805-821.
3. Bassett DS, Bullmore ET, Meyer-Lindenberg A, Apud JA, Weinberger DR, Coppola R. 2009. Cognitive fitness of cost-efficient brain functional networks. Proc Natl Acad Sci USA. 106:11747-11752.
4. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. 2007. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage. 34:144-155.
5. Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O et al. 2003. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 6:750-757.
6. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM. 2003. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. 50:1077-1088.
7. Bigos KL, Weinberger DR. 2010. Imaging genetics-days of future past. Neuroimage. 53:804-809.
8. Boccaletti S, Latora V, Moreno Y, Chavez M, Hwang DU. 2006. Complex networks: structure and dynamics. Phys Rep. 424:175-308.
9. Brandon NJ, Millar JK, Korth C, Sive H, Singh KK, Sawa A. 2009. Understanding the role of DISC1 in psychiatric disease and during normal development. J Neurosci. 29:12768-12775.
10. Brandon NJ, Sawa A. 2011. Linking neurodevelopmental and synaptic theories of mental illness through DISC1. Nat Rev Neurosci. 12:707-722.
11. Bullmore E, Sporns O. 2009. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 10:186-198.
12. Burdick KE, Kamiya A, Hodgkinson CA, Lencz T, DeRosse P, Ishizuka K, Elashvili S, Arai H, Goldman D, Sawa A et al. 2008. Elucidating the relationship between DISC1, NDEL1 and NDE1 and the risk for schizophrenia: evidence of epistasis and competitive binding. Hum Mol Genet. 17:2462-2473.
13. Callicott JH, Straub RE, Pezawas L, Egan MF, Mattay VS, Hariri AR, Verchinski BA, Meyer-Lindenberg A, Balkissoon R, Kolachana B et al. 2005. Variation in DISC1 affects hippocampal structure and function and increases risk for schizophrenia. Proc Natl Acad Sci USA. 102:8627-8632.
14. Chen SY, Huang PH, Cheng HJ. 2011. Disrupted-in-Schizophrenia 1-mediated axon guidance involves TRIO-RAC-PAK small GTPase pathway signaling. Proc Natl Acad Sci USA. 108:5861-5866.
15. DeRosse P, Hodgkinson CA, Lencz T, Burdick KE, Kane JM, Goldman D, Malhotra AK. 2007. Disrupted in schizophrenia 1 genotype and positive symptoms in schizophrenia. Biol Psychiatry. 61:1208-1210.
16. Di Giorgio A, Blasi G, Sambataro F, Rampino A, Papazacharias A, Gambi F, Romano R, Caforio G, Rizzo M, Latorre V et al. 2008. Association of the SerCys DISC1 polymorphism with human hippocampal formation gray matter and function during memory encoding. Eur J Neurosci. 28:2129-2136.
17. Gong G, He Y, Concha L, Lebel C, Gross DW, Evans AC, Beaulieu C. 2009. Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cereb Cortex. 19:524-536.
18. Gong G, Rosa-Neto P, Carbonell F, Chen ZJ, He Y, Evans AC. 2009. Age-and gender-related differences in the cortical anatomical network. J Neurosci. 29:15684-15693.
19. Gong YX. 1982. Manual of modified Wechsler Adult Intelligence Scale (WAIS-RC) (in Chinese). Changsha, China: Hunan Med College.
20. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O. 2008. Mapping the structural core of human cerebral cortex. PLoS Biol. 6:e159.
21. Hagmann P, Kurant M, Gigandet X, Thiran P, Wedeen VJ, Meuli R, Thiran JP. 2007. Mapping human whole-brain structural networks with diffusion MRI. PLoS One. 2:e597.
22. Hashimoto R, Numakawa T, Ohnishi T, Kumamaru E, Yagasaki Y, Ishimoto T, Mori T, Nemoto K, Adachi N, Izumi A et al. 2006. Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum Mol Genet. 15:3024-3033.
23. He Y, Evans A. 2010. Graph theoretical modeling of brain connectivity. Curr Opin Neurol. 23:341-350.
24. Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, Calabresi PA, Pekar JJ, van Zijl PC, Mori S. 2008. Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tractspecific quantification. Neuroimage. 39:336-347.
25. Hulshoff Pol HE, Schnack HG, Mandl RC, Brans RG, van Haren NE, Baare WF, van Oel CJ, Collins DL, Evans AC, Kahn RS. 2006. Gray and white matter density changes in monozygotic and same-sex dizygotic twins discordant for schizophrenia using voxel-based morphometry. Neuroimage. 31:482-488.
26. Iturria-Medina Y, Perez Fernandez A, Morris DM, Canales-Rodriguez EJ, Haroon HA, Garcia Penton L, Augath M, Galan Garcia L, Logothetis N, Parker GJ et al. 2011. Brain hemispheric structural efficiency and interconnectivity rightward asymmetry in human and nonhuman primates. Cereb Cortex. 21:56-67.
27. Iturria-Medina Y, Sotero RC, Canales-Rodriguez EJ, Aleman-Gomez Y, Melie-Garcia L. 2008. Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory. Neuroimage. 40:1064-1076.
28. Johansen-Berg H, Behrens TE, Robson MD, Drobnjak I, Rushworth MF, Brady JM, Smith SM, Higham DJ, Matthews PM. 2004. Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc Natl Acad Sci USA. 101:13335-13340.
29. Johansen-Berg H, Behrens TE, Sillery E, Ciccarelli O, Thompson AJ, Smith SM, Matthews PM. 2005. Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex. 15:31-39.
30. Johnstone M, Thomson PA, Hall J, McIntosh AM, Lawrie SM, Porteous DJ. 2011. DISC1 in schizophrenia: genetic mouse models and human genomic imaging. Schizophr Bull. 37:14-20.
31. Jones DK, Symms MR, Cercignani M, Howard RJ. 2005. The effect of filter size on VBM analyses of DT-MRI data. Neuroimage. 26:546-554.
32. Jung RE, Haier RJ. 2007. The parieto-frontal integration theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci. 30:135-154; discussion 154-187.
33. Kamiya A, Tomoda T, Chang J, Takaki M, Zhan C, Morita M, Cascio MB, Elashvili S, Koizumi H, Takanezawa Y et al. 2006. DISC1-NDEL1/NUDEL protein interaction, an essential component for neurite outgrowth, is modulated by genetic variations of DISC1. Hum Mol Genet. 15:3313-3323.
34. Latora V, Marchiori M. 2001. Efficient behavior of small-world networks. Phys Rev Lett. 87:198701.
35. Li J, Yu C, Li Y, Liu B, Liu Y, Shu N, Song M, Zhou Y, Zhu W, Li K et al. 2009. COMT val158met modulates association between brain white matter architecture and IQ. Am J Med Genet B Neuropsychiatr Genet. 150B:375-380.
36. Li Y, Liu Y, Li J, Qin W, Li K, Yu C, Jiang T. 2009. Brain anatomical network and intelligence. PLoS Comput Biol. 5:e1000395.
37. Liu Y, Liang M, Zhou Y, He Y, Hao Y, Song M, Yu C, Liu H, Liu Z, Jiang T. 2008. Disrupted small-world networks in schizophrenia. Brain. 131:945-961.
38. Mathieson I, Munafo MR, Flint J. 2012. Meta-analysis indicates that common variants at the DISC1 locus are not associated with schizophrenia. Mol Psychiatry. 17:634-641.
39. Mattay VS, Goldberg TE, Sambataro F, Weinberger DR. 2008. Neurobiology of cognitive aging: insights from imaging genetics. Biol Psychol. 79:9-22.
40. Meyer-Lindenberg A. 2010. Imaging genetics of schizophrenia. Dialogues Clin Neurosci. 12:449-456.
41. Micheloyannis S, Pachou E, Stam CJ, Breakspear M, Bitsios P, Vourkas M, Erimaki S, Zervakis M. 2006. Small-world networks and disturbed functional connectivity in schizophrenia. Schizophr Res. 87:60-66.
42. Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L, Fredericksen K, Pearlson GD, Melhem ER, Solaiyappan M, Raymond GV et al. 2002. Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med. 47:215-223.
43. Mori S, Zhang J. 2006. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron. 51:527-539.
44. Qu M, Tang F, Yue W, Ruan Y, Lu T, Liu Z, Zhang H, Han Y, Zhang D, Wang F. 2007. Positive association of the disrupted-inschizophrenia-1 gene (DISC1) with schizophrenia in the Chinese Han population. Am J Med Genet B Neuropsychiatr Genet. 144B:266-270.
45. Shu N, Liu Y, Li J, Li Y, Yu C, Jiang T. 2009. Altered anatomical network in early blindness revealed by diffusion tensor tractography. PLoS One. 4:e7228.
46. Singh KK, De Rienzo G, Drane L, Mao Y, Flood Z, Madison J, Ferreira M, Bergen S, King C, Sklar P et al. 2011. Common DISC1 polymorphisms disrupt Wnt/GSK3beta signaling and brain development. Neuron. 72:545-558.
47. Skudlarski P, Jagannathan K, Anderson K, Stevens MC, Calhoun VD, Skudlarska BA, Pearlson G. 2010. Brain connectivity is not only lower but different in schizophrenia: a combined anatomical and functional approach. Biol Psychiatry. 68:61-69.
48. Sprooten E, Sussmann JE, Moorhead TW, Whalley HC, Ffrench-Constant C, Blumberg HP, Bastin ME, Hall J, Lawrie SM, McIntosh AM. 2011. Association of white matter integrity with genetic variation in an exonic DISC1 SNP. Mol Psychiatry. 16:685; 688-689.
49. Strogatz SH. 2001. Exploring complex networks. Nature. 410:268-276.
50. Sussmann JE, Lymer GK, McKirdy J, Moorhead TW, Munoz Maniega S, Job D, Hall J, Bastin ME, Johnstone EC, Lawrie SM et al. 2009. White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disord. 11:11-18.
51. Thomas G, Sinville R, Sutton S, Farquar H, Hammer RP, Soper SA, Cheng YW, Barany F. 2004. Capillary and microelectrophoretic separations of ligase detection reaction products produced from low-abundant point mutations in genomic DNA. Electrophoresis. 25:1668-1677.
52. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M. 2002. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 15:273-289.
53. van den Heuvel MP, Mandl RC, Stam CJ, Kahn RS, Hulshoff Pol HE. 2010. Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J Neurosci. 30:15915-15926.
54. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P et al. 2007. Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage. 36:630-644.
55. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. 2004. Fiber tract-based atlas of human white matter anatomy. Radiology. 230:77-87.
56. Wang Q, Su TP, Zhou Y, Chou KH, Chen IY, Jiang T, Lin CP. 2012. Anatomical insights into disrupted small-world networks in schizophrenia. Neuroimage. 59:1085-1093.
57. Watts DJ, Strogatz SH. 1998. Collective dynamics of 'small-world' networks. Nature. 393:440-442.
58. Witelson SF. 1989. Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. Brain. 112 (Pt 3):799-835.
59. Wood JD, Bonath F, Kumar S, Ross CA, Cunliffe VT. 2009. Disrupted-in-schizophrenia 1 and neuregulin 1 are required for the specification of oligodendrocytes and neurones in the zebrafish brain. Hum Mol Genet. 18:391-404.
60. Yi P, Chen Z, Zhao Y, Guo J, Fu H, Zhou Y, Yu L, Li L. 2009. PCR/LDR/capillary electrophoresis for detection of single-nucleotide differences between fetal and maternal DNA in maternal plasma. Prenat Diagn. 29:217-222.
61. Zalesky A, Fornito A, Seal ML, Cocchi L, Westin CF, Bullmore ET, Egan GF, Pantelis C. 2011. Disrupted axonal fiber connectivity in schizophrenia. Biol Psychiatry. 69:80-89.