Neuroanatomy of auditory verbal hallucinations in schizophrenia: A quantitative meta-analysis of voxel-based morphometry studies

Cortex

Volumn 49, Issue 4, 2013, Pages 1046-1055

  Modinos, Gemma ^a   Costafreda, Sergi G ^a   Van Tol, Marie José ^b   McGuire, Philip K ^a   Aleman, André ^b   Allen, Paul ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Grey matter volume; Meta analysis; Psychosis; Schizophrenia; Structural MRI

Indexed keywords

ARTICLE; AUDITORY HALLUCINATION; AUDITORY VERBAL HALLUCINATION; BRAIN REGION; DISEASE ASSOCIATION; DISEASE SEVERITY; GRAY MATTER; HUMAN; LANGUAGE PROCESSING; META ANALYSIS; NEUROANATOMY; QUANTITATIVE ANALYSIS; SCHIZOPHRENIA; SUPERIOR TEMPORAL GYRUS; SYMPTOM; VOXEL BASED MORPHOMETRY;

BRAIN; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; FUNCTIONAL LATERALITY; HALLUCINATIONS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; SAMPLE SIZE; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; TEMPORAL LOBE;

EID: 84875809463     PISSN: 00109452     EISSN: 19738102     Source Type: Journal    
DOI: 10.1016/j.cortex.2012.01.009     Document Type: Article

References (84)

1. Aguilar E.J., Sanjuan J., García-Martí G., Lull J.J., Robles M. MR and genetics in schizophrenia: Focus on auditory hallucinations. European Journal of Radiology 2008, 67(3):434-439.
2. Aleman A., Sommer I.E., Kahn R.S. Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: A meta-analysis. Journal of Clinical Psychiatry 2007, 68(3):416-421.
3. Allen P., Larøi F., McGuire P.K., Aleman A. The hallucinating brain: A review of structural and functional neuroimaging studies of hallucinations. Neuroscience and Biobehavioral Reviews 2008, 32(1):175-191.
4. Andreasen N.C., Flaum M. Schizophrenia: The characteristic symptoms. Schizophrenia Bulletin 1991, 17(1):27-49.
5. Andreasen N.C., Flaum M., Arndt S. The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. Archives of General Psychiatry 1992, 49(8):615-623.
6. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11(6 Pt 1):805-821.
7. Ashtari M., Cottone J., Ardekani B.A., Cervellione K., Szeszko P.R., Wu J., et al. Disruption of white matter integrity in the inferior longitudinal fasciculus in adolescents with schizophrenia as revealed by fiber tractography. Archives of General Psychiatry 2007, 64(11):1270-1280.
8. Barta P.E., Pearlson G.D., Powers R.E., Richards S.S., Tune L.E. Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. American Journal of Psychiatry 1990, 147(11):1457-1462.
9. Begré S., Koenig T. Cerebral disconnectivity: An early event in schizophrenia. Neuroscientist 2008, 14(1):19-45.
10. Bora E., Fornito A., Radua J., Walterfang M., Seal M., Wood S.J., et al. Neuroanatomical abnormalities in schizophrenia: A multimodal voxelwise meta-analysis and meta-regression analysis. Schizophrenia Research 2011, 127(1-3):46-57.
11. Braun C.M., Dumont M., Duval J., Hamel-Hebert I., Godbout L. Brain modules of hallucination: An analysis of multiple patients with brain lesions. Journal of Psychiatry and Neuroscience 2003, 28(6):432-449.
12. Brett M., Johnsrude I.S., Owen A.M. The problem of functional localization in the human brain. Nature Reviews. Neuroscience 2002, 3(3):243-249.
13. Casanova R., Srikanth R., Baer A., Laurienti P.J., Burdette J.H., Hayasaka S., et al. Biological parametric mapping: A statistical toolbox for multimodality brain image analysis. NeuroImage 2007, 34(1):137-143.
14. Chibbaro G., Daniele M., Alagona G., Di P.C., Cannavo M., Rapisarda V., et al. Repetitive transcranial magnetic stimulation in schizophrenic patients reporting auditory hallucinations. Neuroscience Letters 2005, 383(1-2):54-57.
15. Costafreda S.G. Pooling fMRI data: Meta-analysis, mega-analysis and multi-center studies. Frontiers in Neuroinformatics 2009, 3:33.
16. Costafreda S.G., David A.S., Brammer M.J. A parametric approach to voxel-based meta-analysis. NeuroImage 2009, 46(1):115-122.
17. d'Alfonso A.A., Aleman A., Kessels R.P., Schouten E.A., Postma A., van Der Linden J.A., et al. Transcranial magnetic stimulation of left auditory cortex in patients with schizophrenia: Effects on hallucinations and neurocognition. Journal of Neuropsychiatry and Clinical Neuroscience 2002, 14(1):77-79.
18. Downar J., Crawley A.P., Mikulis D.J., Davis K.D. A multimodal cortical network for the detection of changes in the sensory environment. Nature Neuroscience 2000, 3(3):277-283.
19. Flaum M., O'Leary D.S., Swayze V.W., Miller D.D., Arndt S., Andreasen N.C. Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders. Journal of Psychiatric Research 1995, 29(4):261-276.
20. Freitas C., Fregni F., Pascual-Leone A. Meta-analysis of the effects of repetitive transcranial magnetic stimulation (rTMS) on negative and positive symptoms in schizophrenia. Schizophrenia Research 2009, 108(1-3):11-24.
21. Frith C.D., Done D.J. Towards a neuropsychology of schizophrenia. British Journal of Psychiatry 1998, 153:437-443.
22. Fusar-Poli P., Borgwardt S., Crescini A., Deste G., Kempton M.J., Lawrie S., et al. Neuroanatomy of vulnerability to psychosis: A voxel-based meta-analysis. Neuroscience and Biobehavioral Reviews 2011, 35(5):1175-1185.
23. García-Martí G., Aguilar E.J., Lull J.J., Martí-Bonmatí L., Escartí M.J., Manjón J.V., et al. Schizophrenia with auditory hallucinations: A voxel-based morphometry study. Progress in Neuropsychopharmacology & Biological Psychiatry 2008, 32(1):72-80.
24. Gaser C., Nenadic I., Volz H.P., Büchel C., Sauer H. Neuroanatomy of " hearing voices" : A frontotemporal brain structural abnormality associated with auditory hallucinations in schizophrenia. Cerebral Cortex 2004, 14(1):91-96.
25. Gaser C., Volz H.P., Sauer H. Deformation based morphometry of auditory hallucinations in schizophrenia. NeuroImage 1999, 9(6 Pt 2):s618.
26. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 2001, 14(1 Pt 1):21-36.
27. Hayasaka S., Nichols T.E. Validating cluster size inference: Random field and permutation methods. NeuroImage 2003, 20(4):2343-2356.
28. Henze R., Brunner R., Thiemann U., Parzer P., Richterich A., Essig M., et al. Grey matter alterations in first-admission adolescents with schizophrenia. Journal of Neuroimaging 2011, 21(3):241-246.
29. Ho B.C., Andreasen N.C., Ziebell S., Pierson R., Magnotta V. Long-term antipsychotic treatment and brain volumes: A longitudinal study of first-episode schizophrenia. Archives of General Psychiatry 2011, 68(2):128-137.
30. Hoffman R.E. Auditory/Verbal hallucinations, speech perception neurocircuitry, and the social deafferentation hypothesis. Clinical EEG and Neuroscience 2008, 39(2):87-90.
31. Hoffman R.E., Gueorguieva R., Hawkins K.A., Varanko M., Boutros N.N., Wu Y.T., et al. Temporoparietal transcranial magnetic stimulation for auditory hallucinations: Safety, efficacy and moderators in a fifty patient sample. Biological Psychiatry 2005, 58(2):97-104.
32. Hoffman R.E., Hawkins K.A., Gueorguieva R., Boutros N.N., Rachid F., Carroll K., et al. Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Archives of General Psychiatry 2003, 60(1):46-59.
33. Honea R., Crow T.J., Passingham D., Mackay C.E. Regional deficits in brain volume in schizophrenia: A meta-analysis of voxel-based morphometry studies. American Journal of Psychiatry 2005, 162(12):2233-2245.
34. Hubl D., Dougoud-Chauvin V., Zeller M., Federspiel A., Boesch C., Strik W., et al. Structural analysis of Heschl's gyrus in schizophrenia patients with auditory hallucinations. Neuropsychobiology 2010, 61(1):1-9.
35. Hubl D., Koenig T., Strik W., Federspiel A., Kreis R., Boesch C., et al. Pathways that make voices: White matter changes in auditory hallucinations. Archives of General Psychiatry 2004, 61(1):658-668.
36. Hugdahl K., Løberg E.M., Specht K., Steen V.M., van Wageningen H., Jørgensen H.A. Auditory hallucinations in schizophrenia: The role of cognitive, brain structural and genetic disturbances in the left temporal lobe. Frontiers in Human Neuroscience 2007, 1:6.
37. Jardri R., Pouchet A., Pins D., Thomas P. Cortical activations during auditory verbal hallucinations in schizophrenia: A coordinate-based meta-analysis. American Journal of Psychiatry 2011, 168(1):73-81.
38. Kleinschmidt A., Falkai P., Huang Y., Schneider T., Fürst G., Steinmetz H. In vivo morphometry of planum temporale asymmetry in first-episode schizophrenia. Schizophrenia Research 1994, 12(1):9-18.
39. Koutsouleris N., Gaser C., Jäger M., Bottlender R., Frodl T., Holzinger S., et al. Structural correlates of psychopathological symptom dimensions in schizophrenia: A voxel-based morphometric study. NeuroImage 2008, 39(4):1600-1612.
40. Lee S.H., Kim W., Chung Y.C., Jung K.H., Bahk W.M., Jun T.Y., et al. A double blind study showing that two weeks of daily repetitive TMS over the left or right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinations. Neuroscience Letters 2005, 376(3):177-181.
41. Lennox B.R., Park S.B., Jones P.B., Morris P.G. Spatial and temporal mapping of neural activity associated with auditory hallucinations. Lancet 1999, 353(9153):644.
42. Lennox B.R., Park S.B., Medley I., Morris P.G., Jones P.B. The functional anatomy of auditory hallucinations in schizophrenia. Psychiatry Research 2000, 100(1):13-20.
43. Lui S., Deng W., Huang X., Jiang L., Ma X., Chen H., et al. Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: An optimized voxel-based morphometry and resting state functional connectivity study. American Journal of Psychiatry 2009, 166(2):196-205.
44. Martí-Bonmatí L., Lull J.J., García-Martí G., Aguilar E.J., Moratal-Pérez D., Poyatos C., et al. Chronic auditory hallucinations in schizophrenic patients: MR analysis of the coincidence between functional and morphologic abnormalities. Radiology 2007, 244(2):549-556.
45. Mechelli A., Price C.J., Friston K.J., Ashburner J. Voxel-based morphometry of the human brain: Methods and applications. Current Medical Imaging Reviews 2005, 1(2):105-113.
46. Modinos G., Vercammen A., Mechelli A., Knegtering H., McGuire P.K., Aleman A. Structural covariance in the hallucinating brain: A voxel-based morphometry study. Journal of Psychiatry and Neuroscience 2009, 34(6):465-469.
47. Moher D., Liberati A., Tetzlaff J., Altman D.G., PRISMA Group Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. BMJ (Clinical Research Ed.) 2009, 339:b2535.
48. Navari S., Dazzan P. Do antipsychotic drugs affect brain structure? A systematic and critical review of MRI findings. Psychological Medicine 2009, 39(11):1763-1777.
49. Nayani T.H., David A.S. The auditory hallucination: A phenomenological survey. Psychological Medicine 1996, 26(1):177-189.
50. Neckelmann G., Specht K., Lund A., Ersland L., Smievoll A.I., Neckelmann D., et al. Mr morphometry analysis of grey matter volume reduction in schizophrenia: Association with hallucinations. International Journal of Neuroscience 2006, 116(1):9-23.
51. Nenadic I., Sauer H., Gaser C. Distinct pattern of brain structural deficits in subsyndromes of schizophrenia delineated by psychopathology. NeuroImage 2010, 49(2):1153-1160.
52. Nenadic I., Smesny S., Schlösser R.G., Sauer H., Gaser C. Auditory hallucinations and brain structure in schizophrenia: Voxel-based morphometric study. British Journal of Psychiatry 2010, 196(5):412-413.
53. O'Daly O.G., Frangou S., Chitnis X., Shergill S.S. Brain structural changes in schizophrenia patients with persistent hallucinations. Psychiatry Research 2007, 156(1):15-21.
54. Onitsuka T., Shenton M.E., Salisbury D.F., Dickey C.C., Kasai K., Toner S.K., et al. Middle and inferior temporal gyrus grey matter volume abnormalities in chronic schizophrenia: An MRI study. American Journal of Psychiatry 2004, 161(9):1603-1611.
55. Parellada E., Lomena F., Font M., Pareto D., Gutierrez F., Simo M., et al. Fluordeoxyglucose-PET study in first-episode schizophrenic patients during the hallucinatory state, after remission and during linguistic-auditory activation. Nuclear Medicine Communications 2008, 29(10):894-900.
56. Pettersson-Yeo W., Allen P., Benetti S., McGuire P., Mechelli A. Dysconnectivity in schizophrenia: Where are we now?. Neuroscience and Biobehavioral Reviews 2011, 35(5):1110-1124.
57. Plaze M., Bartrés-Faz D., Martinot J.L., Januel D., Bellivier F., De Beaurepaire R., et al. Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients. Schizophrenia Research 2006, 87(1-3):109-115.
58. Plaze M., Paillère-Martinot M.L., Penttilä J., Januel D., de Beaurepaire R., Bellivier F., et al. " Where do auditory hallucinations come from?" - a brain morphometry study of schizophrenia patients with inner or outer space hallucinations. Schizophrenia Bulletin 2011, 37(1):212-221.
59. Poulet E., Brunelin J., Bediou B., Bation R., Forgeard L., Dalery J., et al. Slow transcranial magnetic stimulation can rapidly reduce resistant auditory hallucinations in schizophrenia. Biological Psychiatry 2005, 57(2):188-191.
60. Radua J., van den Heuvel O.A., Surguladze S., Mataix-Cols D. Meta-analytical comparison of voxel-based morphometry studies in obsessive-compulsive disorder vs other anxiety disorders. Archives of General Psychiatry 2010, 67(7):701-711.
61. R Development Core Team R: A Language and Environment for Statistical Computing 2005, R Foundation for Statistical Computing, Vienna, Austria.
62. Salimi-Khorshidi G., Smith S.M., Keltner J.R., Wager T.D., Nichols T.E. Meta-analysis of neuroimaging data: A comparison of image-based and coordinate-based pooling of studies. NeuroImage 2009, 45(3):810-823.
63. Seok J.H., Park H.J., Chun J.W., Lee S.K., Cho H.S., Kwon J.S., et al. White matter abnormalities associated with auditory hallucinations in schizophrenia: A combined study of voxel-based analyses of diffusion tensor imaging and structural magnetic resonance imaging. Psychiatry Research 2007, 156(2):93-104.
64. Shapleske J., Rossell S.L., Chitnis X.A., Suckling J., Simmons A., Bullmore E.T., et al. A computational morphometric MRI study of schizophrenia: Effects of hallucinations. Cerebral Cortex 2002, 12(12):1331-1341.
65. Shergill S.S., Brammer M.J., Williams S.C., Murray R.M., McGuire P.K. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Archives of General Psychiatry 2000, 57(11):1033-1038.
66. Shergill S.S., Kanaan R.A., Chitnis X.A., O'Daly O., Jones D.K., Frangou S., et al. A diffusion tensor imaging study of fasciculi in schizophrenia. American Journal of Psychiatry 2007, 164(3):467-473.
67. Shergill S.S., Murray R.M., McGuire P.K. Auditory hallucinations: A review of psychological treatments. Schizophrenia Research 1998, 32(3):137-150.
68. Shin S.E., Lee J.S., Kang M.H., Kim C.E., Bae J.N., Jung G. Segmented volumes of cerebrum and cerebellum in first episode schizophrenia with auditory hallucinations. Psychiatry Research 2005, 138(1):33-42.
69. Slotema C.W., Blom J.D., de Weijer A.D., Diederen K.M., Goekoop R., Looijestijn J., et al. Can low-frequency repetitive transcranial magnetic stimulation really relieve medication-resistant auditory verbal hallucinations? Negative results from a large randomized controlled trial. Biological Psychiatry 2011, 69(5):450-456.
70. Smieskova R., Fusar-Poli P., Allen P., Bendfeldt K., Stieglitz R.D., Drewe J., et al. The effects of antipsychotics on the brain: What have we learnt from structural imaging of schizophrenia? - a systematic review. Current Pharmaceutical Design 2009, 15(22):2535-2549.
71. Spaniel F., Horáček J., Tintěra J., Ibrahim I., Novák T., Cermák J., et al. Genetic variation in FOXP2 alters grey matter concentrations in schizophrenia patients. Neuroscience Letters 2011, 493(3):131-135.
72. Spencer M.D., Moorhead T.W., McIntosh A.M., Stanfield A.C., Muir W.J., Hoare P., et al. Grey matter correlates of early psychotic symptoms in adolescents at enhanced risk of psychosis: A voxel-based study. NeuroImage 2007, 35(3):1181-1191.
73. Stanfield A.C., Moorhead T.W., Job D.E., McKirdy J., Sussmann J.E., Hall J., et al. Structural abnormalities of ventrolateral and orbitofrontal cortex in patients with familial bipolar disorder. Bipolar Disorders 2009, 11(2):135-144.
74. Stroup D.F., Berlin J.A., Morton S.C., Olkin I., Williamson G.D., Rennie D., et al. Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA: the Journal of the American Medical Association 2000, 283(15):2008-2012.
75. Sumich A., Chitnis X.A., Fannon D.G., O'Ceallaigh S., Doku V.C., Faldrowicz A., et al. Unreality symptoms and volumetric measures of Heschl's gyrus and planum temporal in first-episode psychosis. Biological Psychiatry 2005, 57(8):947-950.
76. Sun J., Maller J.J., Guo L., Fitzgerald P.B. Superior temporal gyrus volume change in schizophrenia: A review on region of interest volumetric studies. Brain Research Reviews 2009, 61(1):14-32.
77. Szeszko P.R., Robinson D.G., Ashtari M., Vogel J., Betensky J., Sevy S., et al. Clinical and neuropsychological correlates of white matter abnormalities in recent onset schizophrenia. Neuropsychopharmacology 2008, 33(5):976-984.
78. Turkeltaub P.E., Eden G.F., Jones K.M., Zeffiro T.A. Meta-analysis of the functional neuroanatomy of single-word reading: Method and validation. NeuroImage 2002, 16(3 Pt 1):765-780.
79. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15(1):273-289.
80. Vercammen A., Knegtering H., Bruggeman R., Westenbroek H.M., Jenner J.A., Slooff C.J., et al. Effects of bilateral repetitive transcranial magnetic stimulation on treatment resistant auditory-verbal hallucinations in schizophrenia: A randomized controlled trial. Schizophrenia Research 2009, 114(1-3):172-179.
81. van Tol MJ, Modinos G, Bruggeman R, Knegtering H, and Aleman A. Voxel based grey and white matter morphometry correlates of auditory verbal hallucinations in the corpus callosum and primary language processing areas, submitted for publication.
82. Waters F, Aleman A, Fernyhough C, and Allen P. Report on the inaugural meeting of the International Consortium on Hallucination Research: A clinical and research update and 16 consensus-set goals for future research. Schizophrenia Bulletin, 2012 Jan 5. [Epub ahead of print].
83. Whitehead A. In Meta-analysis of Controlled Clinical Trials. Statistics in Practice 2002, Wiley, Chichester, England, Chapter 1. pp. 1-10.
84. Wright I.C., McGuire P.K., Poline J.B., Travere J.M., Murray R.M., Frith C.D., et al. A voxel-based method for the statistical analysis of grey and white matter density applied to schizophrenia. NeuroImage 1995, 2(4):244-252.