Advertisement

Genetic variation in the G72 gene is associated with increased frontotemporal fiber tract integrity

  • Thomas Nickl-JockschatEmail author
  • Tony Stöcker
  • Axel Krug
  • Valentin Markov
  • Ivan I. Maximov
  • Ruiwang Huang
  • Frank Schneider
  • Ute Habel
  • Simon B. Eickhoff
  • Klaus Zerres
  • Markus M. Nöthen
  • Marcella Rietschel
  • N. Jon Shah
  • Jens Treutlein
  • Tilo Kircher
Original Paper

Abstract

G72 (syn. DAOA, d-amino acid oxidase activator) is a susceptibility gene for both schizophrenia and bipolar disorder. Diffusion tensor imaging studies hint at changes in fiber tract integrity in both disorders. We aimed to investigate whether a G72 susceptibility haplotype causes changes in fiber tract integrity in young healthy subjects. We compared fractional anisotropy in 47 subjects that were either homozygous for the M23/M24 risk haplotype (n = 20) or homozygous for M23(rs3918342)/M24(rs1421292) wild type (n = 27) using diffusion tensor imaging with 3 T. Tract-based spatial statistics, a method especially developed for diffusion data analysis, was used to delineate the major fiber tracts. We found clusters of increased FA values in homozygous risk haplotype carriers in the right periinsular region and in the right inferior parietal lobe (IPL). We did not find clusters indicating decreased FA values. The insula and the IPL have been implicated in both schizophrenia and bipolar pathophysiology. Increased FA values might reflect changes in dendritic morphology as previously described by in vitro studies. These findings further corroborate the hypothesis that a shared gene pool between schizophrenia and bipolar disorder might lead to neuroanatomic changes that confer an unspecific vulnerability for both disorders.

Keywords

Genetics Imaging Schizophrenia Bipolar I disorder MRI 

Notes

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. 1.
    Nöthen MM, Nieratschker V, Cichon S, Rietschel M (2011) New findings in the genetics of major psychoses. Dialogues Clin Neurosci 12:85–93Google Scholar
  2. 2.
    Cardno AG, Rijsdijk FV, Sham PC, Murray RM, McGuffin P (2002) A twin study of genetic relationships between psychotic symptoms. Am J Psychiatry 159:539–545CrossRefPubMedGoogle Scholar
  3. 3.
    Mortensen PB, Pedersen CB, Melbye M, Mors O, Ewald H (2003) Individual and familial risk factors for bipolar affective disorders in Denmark. Arch Gen Psychiatry 60:1209–1215CrossRefPubMedGoogle Scholar
  4. 4.
    Van Snellenberg JX, de Candia T (2009) Meta-analytic evidence for familial coaggregation of schizophrenia and bipolar disorder. Arch Gen Psychiatry 66:748–755CrossRefPubMedGoogle Scholar
  5. 5.
    Lichtenstein P, Yip BH, Björk C, Pawitan Y, Cannon TD, Sullivan PF, Hultman CM (2009) Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 373:234–239CrossRefPubMedGoogle Scholar
  6. 6.
    Chumakov I, Blumenfeld M, Guerassimenko O, Cavarec L, Palicio M, Abderrahim H, Bougueleret L, Barry C, Tanaka H, La Rosa P, Puech A, Tahri N, Cohen-Akenine A, Delabrosse S, Lissarrague S, Picard FP, Maurice K, Essioux L, Millasseau P, Grel P, Debailleul V, Simon AM, Caterina D, Dufaure I, Malekzadeh K, Belova M, Luan JJ, Bouillot M, Sambucy JL, Primas G, Saumier M, Boubkiri N, Martin-Saumier S, Nasroune M, Peixoto H, Delaye A, Pinchot V, Bastucci M, Guillou S, Chevillon M, Sainz-Fuertes R, Meguenni S, Aurich-Costa J, Cherif D, Gimalac A, Van Duijn C, Gauvreau D, Ouellette G, Fortier I, Raelson J, Sherbatich T, Riazanskaia N, Rogaev E, Raeymaekers P, Aerssens J, Konings F, Luyten W, Macciardi F, Sham PC, Straub RE, Weinberger DR, Cohen N, Cohen D (2002) Genetic and physiological data implicating the new human gene G72 and the gene for D-amino acid oxidase in schizophrenia. Proc Natl Acad Sci USA 99:13675–13680CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Addington AM, Gornick M, Sporn AL, Gogtay N, Greenstein D, Lenane M, Gochman P, Baker N, Balkissoon R, Vakkalanka RK, Weinberger DR, Straub RE, Rapoport JL (2004) Polymorphisms in the 13q33.2 gene G72/G30 are associated with childhood-onset schizophrenia and psychosis not otherwise specified. Biol Psychiatry 55:976–980CrossRefPubMedGoogle Scholar
  8. 8.
    Li D, He L (2007) G72/G30 genes and schizophrenia: a systematic meta-analysis of association studies. Genetics 175:917–922CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Ma J, Sun J, Zhang H, Zhang R, Kang WH, Gao CG, Liu HS, Ma XH, Min ZX, Zhao WX, Ning QL, Wang SH, Zhang YC, Guo TW, Lu SM (2009) Evidence for transmission disequilibrium at the DAOA gene locus in a schizophrenia family sample. Neurosci Lett 462(2):105–108CrossRefPubMedGoogle Scholar
  10. 10.
    Bass NJ, Datta SR, McQuillin A, Puri V, Choudhury K, Thirumalai S, Lawrence J, Quested D, Pimm J, Curtis D, Gurling HM (2009) Evidence for the association of the DAOA (G72) gene with schizophrenia and bipolar disorder but not for the association of the DAO gene with schizophrenia. Behav Brain Funct 5:28CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    Schulze TG, Ohlraun S, Czerski PM, Schumacher J, Kassem L, Deschner M, Gross M, Tullius M, Heidmann V, Kovalenko S, Jamra RA, Becker T, Leszczynska-Rodziewicz A, Hauser J, Illig T, Klopp N, Wellek S, Cichon S, Henn FA, McMahon FJ, Maier W, Propping P, Nöthen MM, Rietschel M (2005) Genotype-phenotype studies in bipolar disorder showing association between the DAOA/G30 locus and persecutory delusions: a first step toward a molecular genetic classification of psychiatric phenotypes. Am J Psychiatry 162:2101–2108CrossRefPubMedGoogle Scholar
  12. 12.
    Rietschel M, Beckmann L, Strohmaier J, Georgi A, Karpushova A, Schirmbeck F, Boesshenz KV, Schmäl C, Bürger C, Jamra RA, Schumacher J, Höfels S, Kumsta R, Entringer S, Krug A, Markov V, Maier W, Propping P, Wüst S, Kircher T, Nöthen MM, Cichon S, Schulze TG (2008) G72 and its association with major depression and neuroticism in large population-based groups from Germany. Am J Psychiatry 165:753–762CrossRefPubMedGoogle Scholar
  13. 13.
    Schumacher J, Abou Jamra R, Becker T, Klopp N, Franke P, Jacob C, Sand P, Fritze J, Ohlraun S, Schulze TG, Rietschel M, Illig T, Propping P, Cichon S, Deckert J, Nöthen MM (2005) Investigation of the DAOA/G30 locus in panic disorder. Mol Psychiatry 10:428–429CrossRefPubMedGoogle Scholar
  14. 14.
    Wang KS, Liu XF, Aragam N (2010) A genome-wide meta-analysis identifies novel loci associated with schizophrenia and bipolar disorder Schizophr Res 124:192–199Google Scholar
  15. 15.
    Berenbaum H, Fujita F (1994) Schizophrenia and personality: exploring the boundaries and connections between vulnerability and outcome. J Abnorm Psychol 103:148–158CrossRefPubMedGoogle Scholar
  16. 16.
    Dinzeo TJ, Docherty NM (2007) Normal personality characteristics in schizophrenia: a review of the literature involving the FFM. J Nerv Ment Dis 195:421–429PubMedGoogle Scholar
  17. 17.
    Kendler KS, Gatz M, Gardner CO, Pedersen NL (2006) Personality and major depression: a Swedish longitudinal, population-based twin study. Arch Gen Psychiatry 63:1113–1120CrossRefPubMedGoogle Scholar
  18. 18.
    Detera-Wadleigh SD, McMahon FJ (2006) G72/G30 in schizophrenia and bipolar disorder: review and meta-analysis. Biol Psychiatry 60:106–114CrossRefPubMedGoogle Scholar
  19. 19.
    Shi J, Badner JA, Gershon ES, Liu C (2008) Allelic association of G72/G30 with schizophrenia and bipolar disorder: a comprehensive meta-analysis. Schizophr Res 98:89–97CrossRefPubMedCentralPubMedGoogle Scholar
  20. 20.
    Seifuddin F, Mahon PB, Judy J, Pirooznia M, Jancic D, Taylor J, Goes FS, Potash JB, Zandi PP (2012) Meta-analysis of genetic association studies on bipolar disorder. Am J Med Genet B Neuropsychiatr Gene 159B:508–518CrossRefGoogle Scholar
  21. 21.
    Mothet JP, Parent AT, Wolosker H, Brady RO Jr, Linden DJ, Ferris CD, Rogawski MA, Snyder SH (2000) d-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc Natl Acad Sci USA 97:4926–4931CrossRefPubMedCentralPubMedGoogle Scholar
  22. 22.
    Sacchi S, Cappelletti P, Giovannardi S, Pollegioni L (2011) Evidence for the interaction of D-amino acid oxidase with pLG72 in a glial cell line. Mol Cell Neurosci 48:20–28CrossRefPubMedGoogle Scholar
  23. 23.
    Drews E, Otte DM, Zimmer A (2012) Involvement of the primate specific gene G72 in schizophrenia: From genetic studies to pathomechanisms. Neurosci Biobehav Rev. doi: 10.1016/j.neubiorev.2012.10.009
  24. 24.
    Korostishevsky M, Kremer I, Kaganovich M, Cholostoy A, Murad I, Muhaheed M, Bannoura I, Rietschel M, Dobrusin M, Bening-Abu-Shach U, Belmaker RH, Maier W, Ebstein RP, Navon R (2006) Transmission disequilibrium and haplotype analyses of the G72/G30 locus: suggestive linkage to schizophrenia in Palestinian Arabs living in the North of Israel. Am J Med Genet B Neuropsychiatr Genet 141B(1):91–95CrossRefPubMedGoogle Scholar
  25. 25.
    Andreou D, Saetre P, Werge T, Andreassen OA, Agartz I, Sedvall GC, Hall H, Terenius L, Jönsson EG (2012) D-amino acid oxidase activator gene (DAOA) variation affects cerebrospinal fluid homovanillic acid concentrations in healthy Caucasians. Eur Arch Psychiatry Clin Neurosci 262:549–556CrossRefPubMedCentralPubMedGoogle Scholar
  26. 26.
    Kvajo M, Dhilla A, Swor DE, Karayiorgou M, Gogos JA (2007) Evidence implicating the candidate schizophrenia/bipolar disorder susceptibility gene G72 in mitochondrial function. Mol Psychiatry 13:685–696CrossRefPubMedGoogle Scholar
  27. 27.
    Chang DT, Reynolds IJ (2006) Differences in mitochondrial movement and morphology in young and mature primary cortical neurons in culture. Neuroscience 141:727–736CrossRefPubMedGoogle Scholar
  28. 28.
    Otte DM, Sommersberg B, Kudin A, Guerrero C, Albayram O, Filiou MD, Frisch P, Yilmaz O, Drews E, Turck CW, Bilkei-Gorzó A, Kunz WS, Beck H, Zimmer A (2011) N-acetyl cysteine treatment rescues cognitive deficits induced by mitochondrial dysfunction in G72/G30 transgenic mice. Neuropsychopharmacology 36:2233–2243CrossRefPubMedCentralPubMedGoogle Scholar
  29. 29.
    Filiou MD, Teplytska L, Otte DM, Zimmer A, Turck CW (2012) Myelination and oxidative stress alterations in the cerebellum of the G72/G30 transgenic schizophrenia mouse model. J Psychiatr Res 46(10):1359–1365CrossRefPubMedGoogle Scholar
  30. 30.
    Cheng L, Hattori E, Nakajima A, Woehrle NS, Opal MD, Zhang C, Grennan K, Dulawa SC, Tang YP, Gershon ES, Liu C (2013) Expression of the G72/G30 gene in transgenic mice induces behavioral changes. Mol Psychiatry. doi: 10.1038/mp.2012.185
  31. 31.
    Schmitt A, Hasan A, Gruber O, Falkai P (2011) Schizophrenia as a disorder of disconnectivity. Eur Arch Psychiatry Clin Neurosci 261:S150–S154CrossRefPubMedGoogle Scholar
  32. 32.
    Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–455CrossRefPubMedGoogle Scholar
  33. 33.
    Ono J, Harada K, Takahashi M, Maeda M, Ikenaka K, Sakurai K, Sakai N, Kagawa T, Fritz-Zieroth B, Nagai T (1995) Differentiation between dysmyelination and demyelination using magnetic resonance diffusional anisotropy. Brain Res 671:141–148CrossRefPubMedGoogle Scholar
  34. 34.
    Gulani V, Webb AG, Duncan ID, Lauterbur PC (2001) Apparent diffusion tensor measurements in myelin-deficient rat spinal cords. Magn Reson Med 45:191–195CrossRefPubMedGoogle Scholar
  35. 35.
    Sakuma H, Nomura Y, Takeda K, Tagami T, Nakagawa T, Tamagawa Y, Ishii Y, Tsukamoto T (1991) Adult and neonatal human brain: diffusional anisotropy and myelination with diffusion-weighted MR imaging. Radiology 180:229–233CrossRefPubMedGoogle Scholar
  36. 36.
    Ellison-Wright I, Bullmore E (2009) Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res 108:3–10CrossRefPubMedGoogle Scholar
  37. 37.
    Ford JM, Mathalon DH, Whitfield S, Faustman WO, Roth WT (2002) Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biol Psychiatry 51:485–492CrossRefPubMedGoogle Scholar
  38. 38.
    Hubl D, Koenig T, Strik W, Federspiel A, Kreis R, Boesch C, Maier SE, Schroth G, Lovblad K, Dierks T (2004) Pathways that make voices: white matter changes in auditory hallucinations. Arch Gen Psychiatry 61:658–668CrossRefPubMedGoogle Scholar
  39. 39.
    Bruno S, Cercignani M, Ron M (2008) White matter abnormalities in bipolar disorder: a voxel-based diffusion tensor imaging study. Bipolar Disord 10:460–468CrossRefPubMedGoogle Scholar
  40. 40.
    Kafantaris V, Kingsley P, Ardekani B, Saito E, Lencz T, Lim K et al (2009) Lower orbital frontal white matter integrity in adolescents with bipolar I disorder. J Am Acad Child Adolesc Psychiatry 48:79–86CrossRefPubMedCentralPubMedGoogle Scholar
  41. 41.
    Versace A, Almeida JRC, Hassel S, Walsh ND, Novelli MKCR, Kupfer DJ et al (2008) Elevated left and reduced right orbitomedial prefrontal fractional anisotropy in adults with bipolar disorder revealed by tract-based spatial statistics. Arch Gen Psychiatry 65:1041–1052CrossRefPubMedCentralPubMedGoogle Scholar
  42. 42.
    Sussmann JE, Lymer GKS, Mckirdy J, Moorhead TWJ, Maniega SM, Job D et al (2009) White matter abnormalities in bipolar disorder and schizophrenia detected using diffusion tensor magnetic resonance imaging. Bipolar Disord 11:11–18CrossRefPubMedGoogle Scholar
  43. 43.
    McDonald C, Bullmore E, Sham P, Chitnis X, Suckling J, MacCabe J, Walshe M, Murray RM (2005) Regional volume deviations of brain structure in schizophrenia and psychotic bipolar disorder: computational morphometry study. Br J Psychiatry 186:369–377CrossRefPubMedGoogle Scholar
  44. 44.
    Ayalew M, Le-Niculescu H, Levey DF, Jain N, Changala B, Patel SD, Winiger E, Breier A, Shekhar A, Amdur R, Koller D, Nurnberger JI, Corvin A, Geyer M, Tsuang MT, Salomon D, Schork NJ, Fanous AH, O’Donovan MC, Niculescu AB (2012) Convergent functional genomics of schizophrenia: from comprehensive understanding to genetic risk prediction. Mol Psychiatry 17:887–905CrossRefPubMedCentralPubMedGoogle Scholar
  45. 45.
    Simon TJ, Ding L, Bish JP, McDonald-McGinn DM, Zackai EH, Gee J (2005) Volumetric, connective, and morphologic changes in the brains of children with chromosome 22q11.2 deletion syndrome: an integrative study. Neuroimage 25:169–180CrossRefPubMedGoogle Scholar
  46. 46.
    Vangberg TR, Skranes J, Dale AM, Martinussen M, Brubakk AM, Haraldseth O (2006) Changes in white matter diffusion anisotropy in adolescents born prematurely. Neuroimage 32:1538–1548CrossRefPubMedGoogle Scholar
  47. 47.
    Jones DK, Symms MR, Cercignani M, Howard RJ (2005) The effect of filter size on VBM analyses of DT-MRI data. The effect of filter size on VBM analyses of DT-MRI data. The effect of filter size on VBM analyses of DT-MRI data. Neuroimage 26:546–554CrossRefPubMedGoogle Scholar
  48. 48.
    Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505CrossRefPubMedGoogle Scholar
  49. 49.
    Jbabdi S, Behrens TE, Smith SM (2010) Crossing fibres in tract-based spatial statistics. Neuroimage 49(1):249–256CrossRefPubMedGoogle Scholar
  50. 50.
    Ennis DB, Kindlmann G (2006) Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images. Magn Reson Med 55(1):136–146CrossRefPubMedGoogle Scholar
  51. 51.
    Krug A, Markov V, Leube D, Zerres K, Eggermann T, Nöthen MM, Skowronek MH, Rietschel M, Kircher T (2008) Genetic variation in the schizophrenia-risk gene neuregulin1 correlates with personality traits in healthy individuals. Eur Psychiatry 23(5):344–349CrossRefPubMedGoogle Scholar
  52. 52.
    Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, Kiefer B, Haase A (2002) Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202–1210CrossRefPubMedGoogle Scholar
  53. 53.
    Smith SM, Johansen-Berg H, Jenkinson M, Rueckert D, Nichols TE, Miller KL, Robson MD, Jones DK, Klein JC, Bartsch AJ, Behrens TE (2007) Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat Protoc 2:499–503CrossRefPubMedGoogle Scholar
  54. 54.
    Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25CrossRefPubMedGoogle Scholar
  55. 55.
    Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335CrossRefPubMedGoogle Scholar
  56. 56.
    Eickhoff SB, Paus T, Caspers S, Grosbras MH, Evans AC, Zilles K, Amunts K (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511–521CrossRefPubMedGoogle Scholar
  57. 57.
    Bürgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29:1092–1105CrossRefPubMedGoogle Scholar
  58. 58.
    Douaud G, Jbabdi S, Behrens TE, Menke RA, Gass A, Monsch AU, Rao A, Whitcher B, Kindlmann G, Matthews PM, Smith S (2011) DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer’s disease. Neuroimage 55(3):880–890CrossRefPubMedGoogle Scholar
  59. 59.
    Sexton CE, Mackay CE, Ebmeier KP (2009) A systematic review of diffusion tensor imaging studies in affective disorders. Biol Psychiatry 66:814–823CrossRefPubMedGoogle Scholar
  60. 60.
    Nickl-Jockschat T, Schneider F, Pagel AD, Laird AR, Fox PT, Eickhoff SB (2011) Progressive pathology is functionally linked to the domains of language and emotion: meta-analysis of brain structure changes in schizophrenia patients. Eur Arch Psychiatry Clin Neurosci 261:S166–S171CrossRefPubMedGoogle Scholar
  61. 61.
    Mechelli A, Allen P, Amaro E Jr, Fu CH, Williams SC, Brammer MJ, Johns LC, McGuire PK (2007) Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations. Hum Brain Mapp 28:1213–1222CrossRefPubMedGoogle Scholar
  62. 62.
    Fletcher PC, Frith CD (2009) Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia. Nat Rev Neurosci 10:48–58CrossRefPubMedGoogle Scholar
  63. 63.
    Strakowski SM, DelBello MP, Adler C, Cecil DM, Sax KW (2000) Neuroimaging in bipolar disorder. Bipolar Disord 2:148–164CrossRefPubMedGoogle Scholar
  64. 64.
    Strakowski SM, Adler CM, Holland SK, Mills N, DelBello MP (2004) A preliminary FMRI study of sustained attention in euthymic, unmedicated bipolar disorder. Neuropsychopharmacology 29:1734–1740CrossRefPubMedGoogle Scholar
  65. 65.
    Strakowski SM, Delbello MP, Adler CM (2005) The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 10:105–116CrossRefPubMedGoogle Scholar
  66. 66.
    Yu K, Cheung C, Leung M, Li Q, Chua S, McAlonan G (2010) Are bipolar disorder and schizophrenia neuroanatomically distinct? An anatomical likelihood meta-analysis. Front Hum Neurosci 4:189CrossRefPubMedCentralPubMedGoogle Scholar
  67. 67.
    Nickl-Jockschat T, Stöcker T, Markov V, Krug A, Huang R, Schneider F, Habel U, Zerres K, Nöthen MM, Treutlein J, Rietschel M, Shah NJ, Kircher T (2012) The impact of a dysbindin schizophrenia susceptibility variant on fiber tract integrity in healthy individuals: a TBSS-based diffusion tensor imaging study. Neuroimage 60:847–853CrossRefPubMedGoogle Scholar
  68. 68.
    Nickl-Jockschat T, Stöcker T, Markov V, Krug A, Huang R, Schneider F, Habel U, Zerres K, Nöthen MM, Treutlein J, Rietschel M, Shah NJ, Kircher T (2014) A Neuregulin-1 schizophrenia susceptibility variant causes perihippocampal fiber tract anomalies in healthy young subjects. Brain Behav 4(2):215–226CrossRefPubMedCentralPubMedGoogle Scholar
  69. 69.
    Grillon ML, Oppenheim C, Varoquaux G, Charbonneau F, Devauchelle AD, Krebs MO, Bayle F, Thirion B, Huron C (2012) Hyperfrontality and hypoconnectivity during refreshing in schizophrenia. Psychiatry Res. doi: 10.1016/j.pscychresns.2012.09.001
  70. 70.
    van der Meer L, de Vos AE, Stiekema AP, Pijnenborg GH, van Tol MJ, Nolen WA, David AS, Aleman A (2012) Insight in schizophrenia: involvement of self-reflection networks? Schizophr BullGoogle Scholar
  71. 71.
    Guo S, Kendrick KM, Yu R, Wang HL, Feng J (2012) Key functional circuitry altered in schizophrenia involves parietal regions associated with sense of self. Hum Brain Mapp. doi: 10.1002/hbm.22162
  72. 72.
    Legrand D, Ruby P (2009) What is self-specific? Theoretical investigation and critical review of neuroimaging results. Psychol Rev 116:252–282CrossRefPubMedGoogle Scholar
  73. 73.
    Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711CrossRefPubMedGoogle Scholar
  74. 74.
    Kircher TT, Leube DT (2003) Self-consciousness, self-agency, and schizophrenia. Conscious Cogn 12:656–669CrossRefPubMedGoogle Scholar
  75. 75.
    Liu CH, Ma X, Li F, Wang YJ, Tie CL, Li SF, Chen TL, Fan TT, Zhang Y, Dong J, Yao L, Wu X, Wang CY (2012) Regional homogeneity within the default mode network in bipolar depression: a resting-state functional magnetic resonance imaging study. PLoS ONE 7(11):e48181. doi: 10.1371/journal.pone.0048181 CrossRefPubMedCentralPubMedGoogle Scholar
  76. 76.
    Thomas LA, Brotman MA, Muhrer EJ, Rosen BH, Bones BL, Reynolds RC, Deveney CM, Pine DS, Leibenluft E (2012) Parametric modulation of neural activity by emotion in youth with bipolar disorder, youth with severe mood dysregulation, and healthy volunteers. Arch Gen Psychiatry 69:1257–1266CrossRefPubMedCentralPubMedGoogle Scholar
  77. 77.
    Mitchell RL, Crow TJ (2005) Right hemisphere language functions and schizophrenia: the forgotten hemisphere? Brain 128:963–978CrossRefPubMedGoogle Scholar
  78. 78.
    Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926CrossRefPubMedCentralPubMedGoogle Scholar
  79. 79.
    Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59(3):2349–2361CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Thomas Nickl-Jockschat
    • 1
    • 2
    Email author
  • Tony Stöcker
    • 2
    • 3
  • Axel Krug
    • 4
  • Valentin Markov
    • 1
  • Ivan I. Maximov
    • 3
  • Ruiwang Huang
    • 2
    • 3
  • Frank Schneider
    • 1
    • 2
  • Ute Habel
    • 1
    • 2
  • Simon B. Eickhoff
    • 5
    • 6
  • Klaus Zerres
    • 7
  • Markus M. Nöthen
    • 8
  • Marcella Rietschel
    • 9
  • N. Jon Shah
    • 2
    • 3
    • 10
  • Jens Treutlein
    • 9
  • Tilo Kircher
    • 4
  1. 1.Department of Psychiatry, Psychotherapy and PsychosomaticsRWTH Aachen UniversityAachenGermany
  2. 2.Juelich Aachen Research Alliance – Translational Brain MedicineJuelichGermany
  3. 3.Institute of Neurosciences and Medicine-4Juelich Research CentreJuelichGermany
  4. 4.Department of Psychiatry and PsychotherapyUniversity of MarburgMarburgGermany
  5. 5.Institute of Clinical Neuroscience and Medical PsychologyHeinrich Heine UniversityDüsseldorfGermany
  6. 6.Department of Neuroscience und Medicine, INM-1Juelich Research CentreJuelichGermany
  7. 7.Institute of Human GeneticsRWTH Aachen UniversityAachenGermany
  8. 8.Department of Genomics, Life & Brain CenterUniversity of BonnBonnGermany
  9. 9.Department of Genetic Epidemiology in PsychiatryCentral Institute of Mental HealthMannheimGermany
  10. 10.Department of NeurologyRWTH Aachen UniversityAachenGermany

Personalised recommendations