Convergent evidence from multimodal imaging reveals amygdala abnormalities in schizophrenic patients and their first-degree relatives

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Tian, Lin ^a,b   Meng, Chun ^c   Yan, Hao ^a,b   Zhao, Qiang ^d   Liu, Qi ^a,b   Yan, Jun ^a,b   Han, Yonghua ^a,b   Yuan, Huishu ^d   Wang, Lifang ^a,b   Yue, Weihua ^a,b   Zhang, Yanbo ^e   Li, Xinmin ^e   Zhu, Chaozhe ^c   He, Yong ^c   Zhang, Dai ^a,b  

^a PEKING UNIVERSITY SIXTH HOSPITAL   (China)

^b BEIJING HOSPITAL   (China)

^c BEIJING NORMAL UNIVERSITY   (China)

^d PEKING UNIVERSITY THIRD HOSPITAL   (China)

^e UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN; BRAIN FUNCTION; BRAIN MALFORMATION; BRAIN STRUCTURE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOPHENOTYPE; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; IMAGING; INSULA; MALE; MENTAL PATIENT; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; ORBITAL CORTEX; PARENT; PRECUNEUS; RELATIVE; SCHIZOPHRENIA; THALAMUS; VOXEL BASED MORPHOMETRY; CASE CONTROL STUDY; CONGENITAL MALFORMATION; DEMOGRAPHY; FAMILY; METHODOLOGY; MIDDLE AGED; NERVE CELL NETWORK; PATHOLOGY; PATHOPHYSIOLOGY;

AMYGDALA; CASE-CONTROL STUDIES; DEMOGRAPHY; FAMILY; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; SCHIZOPHRENIA; YOUNG ADULT;

EID: 82955207192     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028794     Document Type: Article

References (93)

1. Mueser KT, McGurk SR, (2004) Schizophrenia. Lancet 363: 2063-2072.
2. Sawa A, Snyder SH, (2002) Schizophrenia: diverse approaches to a complex disease. Science 296: 692-695.
3. Tsuang M, (2000) Schizophrenia: genes and environment. Biol Psychiatry 47: 210-220.
4. McGuffin P, Owen MJ, Farmer AE, (1995) Genetic basis of schizophrenia. Lancet 346: 678-682.
5. Shenton ME, Dickey CC, Frumin M, McCarley RW, (2001) A review of MRI findings in schizophrenia. Schizophr Res 49: 1-52.
6. Mitchell RL, Elliott R, Woodruff PW, (2001) fMRI and cognitive dysfunction in schizophrenia. Trends Cogn Sci 5: 71-81.
7. Wright IC, Rabe-Hesketh S, Woodruff PW, David AS, Murray RM, et al. (2000) Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157: 16-25.
8. Lawrie SM, Abukmeil SS, (1998) Brain abnormality in schizophrenia. A systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry 172: 110-120.
9. Fornito A, Yucel M, Patti J, Wood SJ, Pantelis C, (2009) Mapping grey matter reductions in schizophrenia: an anatomical likelihood estimation analysis of voxel-based morphometry studies. Schizophr Res 108: 104-113.
10. Williams LM, Das P, Harris AW, Liddell BB, Brammer MJ, et al. (2004) Dysregulation of arousal and amygdala-prefrontal systems in paranoid schizophrenia. Am J Psychiatry 161: 480-489.
11. Takahashi H, Koeda M, Oda K, Matsuda T, Matsushima E, et al. (2004) An fMRI study of differential neural response to affective pictures in schizophrenia. Neuroimage 22: 1247-1254.
12. Potkin SG, Ford JM, (2009) Widespread cortical dysfunction in schizophrenia: the FBIRN imaging consortium. Schizophr Bull 35: 15-18.
13. Habel U, Klein M, Shah NJ, Toni I, Zilles K, et al. (2004) Genetic load on amygdala hypofunction during sadness in nonaffected brothers of schizophrenia patients. Am J Psychiatry 161: 1806-1813.
14. Boos HB, Aleman A, Cahn W, Hulshoff Pol H, Kahn RS, (2007) Brain volumes in relatives of patients with schizophrenia: a meta-analysis. Arch Gen Psychiatry 64: 297-304.
15. Whitfield-Gabrieli S, Thermenos HW, Milanovic S, Tsuang MT, Faraone SV, et al. (2009) Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc Natl Acad Sci U S A 106: 1279-1284.
16. Seidman LJ, Faraone SV, Goldstein JM, Kremen WS, Horton NJ, et al. (2002) Left hippocampal volume as a vulnerability indicator for schizophrenia: a magnetic resonance imaging morphometric study of nonpsychotic first-degree relatives. Arch Gen Psychiatry 59: 839-849.
17. Gottesman II, Gould TD, (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160: 636-645.
18. MacDonald AW 3rd, Thermenos HW, Barch DM, Seidman LJ, (2009) Imaging genetic liability to schizophrenia: systematic review of FMRI studies of patients' nonpsychotic relatives. Schizophr Bull 35: 1142-1162.
19. Atkinson AJ, Colburn WA, DeGruttola VG, DeMets DL, DO GJD, et al. (2001) Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 69: 89-95.
20. Prasad KM, Keshavan MS, (2008) Structural cerebral variations as useful endophenotypes in schizophrenia: do they help construct "extended endophenotypes"? Schizophr Bull 34: 774-790.
21. Stephan KE, Baldeweg T, Friston KJ, (2006) Synaptic plasticity and dysconnection in schizophrenia. Biol Psychiatry 59: 929-939.
22. Friston KJ, (1999) Schizophrenia and the disconnection hypothesis. Acta Psychiatr Scand Suppl 395: 68-79.
23. Stephan KE, Friston KJ, Frith CD, (2009) Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull 35: 509-527.
24. Greicius M, (2008) Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 21: 424-430.
25. Calhoun VD, Eichele T, Pearlson G, (2009) Functional brain networks in schizophrenia: a review. Front Hum Neurosci 3: 17.
26. Wolf DH, Gur RC, Valdez JN, Loughead J, Elliott MA, et al. (2007) Alterations of fronto-temporal connectivity during word encoding in schizophrenia. Psychiatry Res 154: 221-232.
27. Tregellas J, (2009) Connecting brain structure and function in schizophrenia. Am J Psychiatry 166: 134-136.
28. Zhou Y, Shu N, Liu Y, Song M, Hao Y, et al. (2008) Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr Res 100: 120-132.
29. Lui S, Deng W, Huang X, Jiang L, Ma X, et al. (2009) Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. Am J Psychiatry 166: 196-205.
30. van Haren NE, Bakker SC, Kahn RS, (2008) Genes and structural brain imaging in schizophrenia. Curr Opin Psychiatry 21: 161-167.
31. Steel RM, Whalley HC, Miller P, Best JJ, Johnstone EC, et al. (2002) Structural MRI of the brain in presumed carriers of genes for schizophrenia, their affected and unaffected siblings. J Neurol Neurosurg Psychiatry 72: 455-458.
32. Glahn DC, Winkler AM, Kochunov P, Almasy L, Duggirala R, et al. (2010) Genetic control over the resting brain. Proc Natl Acad Sci U S A 107: 1223-1228.
33. Liu H, Kaneko Y, Ouyang X, Li L, Hao Y, et al. (2010) Schizophrenic Patients and Their Unaffected Siblings Share Increased Resting-State Connectivity in the Task-Negative Network but Not Its Anticorrelated Task-Positive Network. Schizophr Bull Available:http://schizophreniabulletin.oxfordjournals.org/content/early/2010/06/30/schbul.sbq074.full.pdfhtml.
34. Glahn DC, Laird AR, Ellison-Wright I, Thelen SM, Robinson JL, et al. (2008) Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biol Psychiatry 64: 774-781.
35. Hulshoff Pol HE, Schnack HG, Mandl RC, van Haren NE, Koning H, et al. (2001) Focal gray matter density changes in schizophrenia. Arch Gen Psychiatry 58: 1118-1125.
36. Seidman LJ, Faraone SV, Goldstein JM, Goodman JM, Kremen WS, et al. (1999) Thalamic and amygdala-hippocampal volume reductions in first-degree relatives of patients with schizophrenia: an MRI-based morphometric analysis. Biol Psychiatry 46: 941-954.
37. Harms MP, Wang L, Mamah D, Barch DM, Thompson PA, et al. (2007) Thalamic shape abnormalities in individuals with schizophrenia and their nonpsychotic siblings. J Neurosci 27: 13835-13842.
38. Job DE, Whalley HC, Johnstone EC, Lawrie SM, (2005) Grey matter changes over time in high risk subjects developing schizophrenia. Neuroimage 25: 1023-1030.
39. Bogerts B, Lieberman JA, Ashtari M, Bilder RM, Degreef G, et al. (1993) Hippocampus-amygdala volumes and psychopathology in chronic schizophrenia. Biol Psychiatry 33: 236-246.
40. Joyal CC, Laakso MP, Tiihonen J, Syvalahti E, Vilkman H, et al. (2003) The amygdala and schizophrenia: a volumetric magnetic resonance imaging study in first-episode, neuroleptic-naive patients. Biol Psychiatry 54: 1302-1304.
41. Velakoulis D, Wood SJ, Wong MT, McGorry PD, Yung A, et al. (2006) Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, first-episode psychosis, and ultra-high-risk individuals. Arch Gen Psychiatry 63: 139-149.
42. Exner C, Boucsein K, Degner D, Irle E, Weniger G, (2004) Impaired emotional learning and reduced amygdala size in schizophrenia: a 3-month follow-up. Schizophr Res 71: 493-503.
43. O'Doherty J, Kringelbach ML, Rolls ET, Hornak J, Andrews C, (2001) Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4: 95-102.
44. O'Driscoll GA, Florencio PS, Gagnon D, Wolff AV, Benkelfat C, et al. (2001) Amygdala-hippocampal volume and verbal memory in first-degree relatives of schizophrenic patients. Psychiatry Res 107: 75-85.
45. Moorhead TW, Stanfield A, Spencer M, Hall J, McIntosh A, et al. (2009) Progressive temporal lobe grey matter loss in adolescents with schizotypal traits and mild intellectual impairment. Psychiatry Res 174: 105-109.
46. Keshavan MS, Dick E, Mankowski I, Harenski K, Montrose DM, et al. (2002) Decreased left amygdala and hippocampal volumes in young offspring at risk for schizophrenia. Schizophr Res 58: 173-183.
47. Lawrie SM, Whalley HC, Job DE, Johnstone EC, (2003) Structural and functional abnormalities of the amygdala in schizophrenia. Ann N Y Acad Sci 985: 445-460.
48. Amunts K, Kedo O, Kindler M, Pieperhoff P, Mohlberg H, et al. (2005) Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat Embryol (Berl) 210: 343-352.
49. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, et al. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15: 273-289.
50. Boos HB, Cahn W, van Haren NE, Derks EM, Brouwer RM, et al. (2011) Focal And Global Brain Measurements in Siblings of Patients With Schizophrenia. Schizophr Bull Available:http://schizophreniabulletin.oxfordjournals.org/content/early/2011/01/17/schbul.sbq147.full.pdf.
51. van Rijn S, Aleman A, Swaab H, Kahn RS, (2005) Neurobiology of emotion and high risk for schizophrenia: role of the amygdala and the X-chromosome. Neurosci Biobehav Rev 29: 385-397.
52. Chan RC, Di X, McAlonan GM, Gong QY, (2011) Brain anatomical abnormalities in high-risk individuals, first-episode, and chronic schizophrenia: an activation likelihood estimation meta-analysis of illness progression. Schizophr Bull 37: 177-188.
53. Hoptman MJ, D'Angelo D, Catalano D, Mauro CJ, Shehzad ZE, et al. (2010) Amygdalofrontal functional disconnectivity and aggression in schizophrenia. Schizophr Bull 36: 1020-1028.
54. Williams LM, Das P, Liddell BJ, Olivieri G, Peduto AS, et al. (2007) Fronto-limbic and autonomic disjunctions to negative emotion distinguish schizophrenia subtypes. Psychiatry Res 155: 29-44.
55. Paradiso S, Andreasen NC, Crespo-Facorro B, O'Leary DS, Watkins GL, et al. (2003) Emotions in unmedicated patients with schizophrenia during evaluation with positron emission tomography. Am J Psychiatry 160: 1775-1783.
56. Phillips ML, Drevets WC, Rauch SL, Lane R, (2003) Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biol Psychiatry 54: 504-514.
57. Phillips ML, Drevets WC, Rauch SL, Lane R, (2003) Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biol Psychiatry 54: 515-528.
58. Jang JH, Jung WH, Choi JS, Choi CH, Kang DH, et al. (2011) Reduced prefrontal functional connectivity in the default mode network is related to greater psychopathology in subjects with high genetic loading for schizophrenia. Schizophr Res 127: 58-65.
59. Venables NC, Bernat EM, Sponheim SR, (2009) Genetic and disorder-specific aspects of resting state EEG abnormalities in schizophrenia. Schizophr Bull 35: 826-839.
60. Pearlson GD, Calhoun VD, (2009) Convergent approaches for defining functional imaging endophenotypes in schizophrenia. Front Hum Neurosci 3: 37.
61. Schlosser RGM, Nenadic I, Wagner G, Gullmar D, von Consbruch K, et al. (2007) White matter abnormalities and brain activation in schizophrenia: A combined DTI and fMRI study. Schizophrenia Research 89: 1-11.
62. Ke M, Huang X, Shen H, Zhou ZT, Chen XG, et al. (2008) Combined analysis of resting-state fMRI and DTI data reveals abnormal development of function-structure in early-onset schizophrenia. Rough Sets and Knowledge Technology 5009: 628-635.
63. Pomarol-Clotet E, Canales-Rodriguez EJ, Salvador R, Sarro S, Gomar JJ, et al. (2010) Medial prefrontal cortex pathology in schizophrenia as revealed by convergent findings from multimodal imaging. Molecular Psychiatry 15: 823-830.
64. Calhoun VD, Adali T, Giuliani NR, Pekar JJ, Kiehl KA, et al. (2006) Method for Multimodal analysis of independent source differences in schizophrenia: Combining gray matter structural and auditory oddball functional data. Human Brain Mapping 27: 47-62.
65. Alstott J, Breakspear M, Hagmann P, Cammoun L, Sporns O, (2009) Modeling the impact of lesions in the human brain. PLoS Comput Biol 5: e1000408.
66. Paus T, Keshavan M, Giedd JN, (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9: 947-957.
67. Niu L, Matsui M, Zhou SY, Hagino H, Takahashi T, et al. (2004) Volume reduction of the amygdala in patients with schizophrenia: a magnetic resonance imaging study. Psychiatry Res 132: 41-51.
68. Bora E, Fornito A, Radua J, Walterfang M, Seal M, et al. (2011) Neuroanatomical abnormalities in schizophrenia: a multimodal voxelwise meta-analysis and meta-regression analysis. Schizophr Res 127: 46-57.
69. Gur RE, McGrath C, Chan RM, Schroeder L, Turner T, et al. (2002) An fMRI study of facial emotion processing in patients with schizophrenia. Am J Psychiatry 159: 1992-1999.
70. Reynolds GP, (1983) Increased concentrations and lateral asymmetry of amygdala dopamine in schizophrenia. Nature 305: 527-529.
71. Qiu A, Wang L, Younes L, Harms MP, Ratnanather JT, et al. (2009) Neuroanatomical asymmetry patterns in individuals with schizophrenia and their non-psychotic siblings. Neuroimage 47: 1221-1229.
72. Bracha HS, (1991) Etiology of structural asymmetry in schizophrenia: an alternative hypothesis. Schizophr Bull 17: 551-553.
73. Gilmore JH, Lin W, Prastawa MW, Looney CB, Vetsa YS, et al. (2007) Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J Neurosci 27: 1255-1260.
74. Honea RA, Meyer-Lindenberg A, Hobbs KB, Pezawas L, Mattay VS, et al. (2008) Is gray matter volume an intermediate phenotype for schizophrenia? A voxel-based morphometry study of patients with schizophrenia and their healthy siblings. Biol Psychiatry 63: 465-474.
75. Seshadri S, DeStefano AL, Au R, Massaro JM, Beiser AS, et al. (2007) Genetic correlates of brain aging on MRI and cognitive test measures: a genome-wide association and linkage analysis in the Framingham Study. BMC Med Genet 8 (Suppl 1): S15.
76. Allison DB, (1997) Transmission-disequilibrium tests for quantitative traits. Am J Hum Genet 60: 676-690.
77. Horvath S, Xu X, Laird NM, (2001) The family based association test method: strategies for studying general genotype-phenotype associations. Eur J Hum Genet 9: 301-306.
78. World Health Organization. (1993) The ICD-10 classification of mental and behavioural disorders: diagnostic criteria for research xiii Geneva World Health Organization.
79. Woods SW, (2003) Chlorpromazine equivalent doses for the newer atypical antipsychotics. Journal of Clinical Psychiatry 64: 663-667.
80. Bai YM, Chen TT, Chen JY, Chang WH, Wu B, et al. (2007) Equivalent switching dose from oral risperidone to risperidone long-acting injection: A 48-week randomized, prospective, single-blind pharmacokinetic study. Journal of Clinical Psychiatry 68: 1218-1225.
81. Lehman AF, Steinwachs DM, Project C-IP, (1998) At issue: Translating research into practice: The Schizophrenia Patient Outcomes Research Team (PORT) treatment recommendations. Schizophrenia Bulletin 24: 1-10.
82. Kay SR, Fiszbein A, Opler LA, (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13: 261-276.
83. Oldfield RC, (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9: 97-113.
84. Salvadore G, Nugent AC, Lemaitre H, Luckenbaugh DA, Tinsley R, et al. (2011) Prefrontal cortical abnormalities in currently depressed versus currently remitted patients with major depressive disorder. Neuroimage 54: 2643-2651.
85. Lui S, Deng W, Huang X, Jiang L, Ouyang L, et al. (2009) Neuroanatomical differences between familial and sporadic schizophrenia and their parents: an optimized voxel-based morphometry study. Psychiatry Res 171: 71-81.
86. McIntosh AM, Job DE, Moorhead TW, Harrison LK, Forrester K, et al. (2004) Voxel-based morphometry of patients with schizophrenia or bipolar disorder and their unaffected relatives. Biol Psychiatry 56: 544-552.
87. Job DE, Whalley HC, McConnell S, Glabus M, Johnstone EC, et al. (2003) Voxel-based morphometry of grey matter densities in subjects at high risk of schizophrenia. Schizophr Res 64: 1-13.
88. Qiu L, Tian L, Pan C, Zhu R, Liu Q, et al. (2011) Neuroanatomical circuitry associated with exploratory eye movement in schizophrenia: a voxel-based morphometric study. PLoS One 6: e25805.
89. Di Martino A, Scheres A, Margulies DS, Kelly AM, Uddin LQ, et al. (2008) Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 18: 2735-2747.
90. Jiang AP, Kennedy DN, Baker JR, Weisskoff RM, Tootell RBH, et al. (1995) Motion detection and correction in functional MR imaging. Human Brain Mapping 3: 224-235.
91. Lowe MJ, Mock BJ, Sorenson JA, (1998) Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7: 119-132.
92. Yan H, Zuo XN, Wang D, Wang J, Zhu C, et al. (2009) Hemispheric asymmetry in cognitive division of anterior cingulate cortex: a resting-state functional connectivity study. Neuroimage 47: 1579-1589.
93. Van Essen DC, (2005) A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28: 635-662.