Functional connectivity of left Heschl's gyrus in vulnerability to auditory hallucinations in schizophrenia

Schizophrenia Research

Volumn 143, Issue 2-3, 2013, Pages 260-268

  Shinn, Ann K ^a,b   Baker, Justin T ^a,b   Cohen, Bruce M ^a,b   Öngür, Dost ^a,b  

^a MCLEAN HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Broca's area; Cingulate cortex; Hippocampus; Mediodorsal thalamus; Psychosis; Resting state fMRI

Indexed keywords

ANTIDEPRESSANT AGENT; ARIPIPRAZOLE; BENZODIAZEPINE; CHLORPROMAZINE; CLOZAPINE; FLUPHENAZINE; HALOPERIDOL; LITHIUM; LOXAPINE; OLANZAPINE; PALIPERIDONE; PERPHENAZINE; QUETIAPINE; RISPERIDONE;

ADULT; AGED; ANATOMICAL VARIATION; ARTICLE; AUDITORY HALLUCINATION; BRAIN FUNCTION; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGONAL BAND OF BROCA; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HESCHL GYRUS; HUMAN; IMAGE ANALYSIS; IMAGE DISPLAY; INFERIOR FRONTAL GYRUS; LANGUAGE; MALE; MEMORY; NEUROIMAGING; ORBITAL CORTEX; OUTCOME ASSESSMENT; POSTCENTRAL GYRUS; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; SCHIZOPHRENIFORM DISORDER; SPEECH; THALAMUS DORSOMEDIAL NUCLEUS;

ADOLESCENT; ADULT; AUDITORY CORTEX; FEMALE; HALLUCINATIONS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; PSYCHOTIC DISORDERS; SCHIZOPHRENIA; SEVERITY OF ILLNESS INDEX; YOUNG ADULT;

EID: 84872400780     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2012.11.037     Document Type: Article

References (69)

1. Allen P., Amaro E., Fu C.H., Williams S.C., Brammer M.J., Johns L.C., McGuire P.K. Neural correlates of the misattribution of speech in schizophrenia. Br. J. Psychiatry 2007, 190:162-169.
2. Allen P., Laroi F., McGuire P.K., Aleman A. The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci. Biobehav. Rev. 2008, 32(1):175-191.
3. Andreasen N.C., Nopoulos P., O'Leary D.S., Miller D.D., Wassink T., Flaum M. Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol. Psychiatry 1999, 46(7):908-920.
4. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360(1457):1001-1013.
5. Carter C.S., Braver T.S., Barch D.M., Botvinick M.M., Noll D., Cohen J.D. Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 1998, 280(5364):747-749.
6. Cohen B.M., Yurgelun-Todd D. Alterations of thalamic activity in schizophrenia and in response to antipsychotic drugs: studies in the legacy of Seymour S. Kety. Neuropsychopharmacology 2001, 25(3):305-312.
7. Copolov D.L., Seal M.L., Maruff P., Ulusoy R., Wong M.T., Tochon-Danguy H.J., Egan G.F. Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: a PET correlation study. Psychiatry Res. 2003, 122(3):139-152.
8. Cordes D., Haughton V.M., Arfanakis K., Carew J.D., Turski P.A., Moritz C.H., Quigley M.A., Meyerand M.E. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am. J. Neuroradiol. 2001, 22(7):1326-1333.
9. Da Costa S., van der Zwaag W., Marques J.P., Frackowiak R.S., Clarke S., Saenz M. Human primary auditory cortex follows the shape of Heschl's gyrus. J. Neurosci. 2011, 31(40):14067-14075.
10. Damoiseaux J.S., Rombouts S.A., Barkhof F., Scheltens P., Stam C.J., Smith S.M., Beckmann C.F. Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(37):13848-13853.
11. Diederen K.M., Neggers S.F., Daalman K., Blom J.D., Goekoop R., Kahn R.S., Sommer I.E. Deactivation of the parahippocampal gyrus preceding auditory hallucinations in schizophrenia. Am. J. Psychiatry 2010, 167(4):427-435.
12. Dierks T., Linden D.E., Jandl M., Formisano E., Goebel R., Lanfermann H., Singer W. Activation of Heschl's gyrus during auditory hallucinations. Neuron 1999, 22(3):615-621.
13. Falloon I.R., Talbot R.E. Persistent auditory hallucinations: coping mechanisms and implications for management. Psychol. Med. 1981, 11(2):329-339.
14. Ford J.M., Roach B.J., Jorgensen K.W., Turner J.A., Brown G.G., Notestine R., Bischoff-Grethe A., Greve D., Wible C., Lauriello J., Belger A., Mueller B.A., Calhoun V., Preda A., Keator D., O'Leary D.S., Lim K.O., Glover G., Potkin S.G., Mathalon D.H. Tuning in to the voices: a multisite FMRI study of auditory hallucinations. Schizophr. Bull. 2009, 35(1):58-66.
15. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8(9):700-711.
16. Frith C.D., Done D.J. Towards a neuropsychology of schizophrenia. Br. J. Psychiatry 1988, 153:437-443.
17. Gavrilescu M., Rossell S., Stuart G.W., Shea T.L., Innes-Brown H., Henshall K., McKay C., Sergejew A.A., Copolov D., Egan G.F. Reduced connectivity of the auditory cortex in patients with auditory hallucinations: a resting state functional magnetic resonance imaging study. Psychol. Med. 2009, 40(7):1149-1158.
18. Haddock G., McCarron J., Tarrier N., Faragher E.B. Scales to measure dimensions of hallucinations and delusions: the psychotic symptom rating scales (PSYRATS). Psychol. Med. 1999, 29(4):879-889.
19. Hazlett E.A., Buchsbaum M.S., Byne W., Wei T.C., Spiegel-Cohen J., Geneve C., Kinderlehrer R., Haznedar M.M., Shihabuddin L., Siever L.J. Three-dimensional analysis with MRI and PET of the size, shape, and function of the thalamus in the schizophrenia spectrum. Am. J. Psychiatry 1999, 156(8):1190-1199.
20. Hazlett E.A., Buchsbaum M.S., Kemether E., Bloom R., Platholi J., Brickman A.M., Shihabuddin L., Tang C., Byne W. Abnormal glucose metabolism in the mediodorsal nucleus of the thalamus in schizophrenia. Am. J. Psychiatry 2004, 161(2):305-314.
21. Hoffman R.E. Revisiting Arieti's "listening attitude" and hallucinated voices. Schizophr. Bull. 2010, 36(3):440-442.
22. Hoffman R.E., Anderson A.W., Varanko M., Gore J.C., Hampson M. Time course of regional brain activation associated with onset of auditory/verbal hallucinations. Br. J. Psychiatry 2008, 193(5):424-425.
23. Hoffman R.E., Fernandez T., Pittman B., Hampson M. Elevated functional connectivity along a corticostriatal loop and the mechanism of auditory/verbal hallucinations in patients with schizophrenia. Biol. Psychiatry 2011, 69(5):407-414.
24. Hugdahl K. "Hearing voices": auditory hallucinations as failure of top-down control of bottom-up perceptual processes. Scand. J. Psychol. 2009, 50(6):553-560.
25. Jakary A., Vinogradov S., Feiwell R., Deicken R.F. N-acetylaspartate reductions in the mediodorsal and anterior thalamus in men with schizophrenia verified by tissue volume corrected proton MRSI. Schizophr. Res. 2005, 76(2-3):173-185.
26. Jardri R., Pouchet A., Pins D., Thomas P. Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Am. J. Psychiatry 2010, 168(1):73-81.
27. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 2002, 17(2):825-841.
28. Jones S.R. Do we need multiple models of auditory verbal hallucinations? Examining the phenomenological fit of cognitive and neurological models. Schizophr. Bull. 2010, 36(3):566-575.
29. Jones S.R., Fernyhough C. Neural correlates of inner speech and auditory verbal hallucinations: a critical review and theoretical integration. Clin. Psychol. Rev. 2007, 27(2):140-154.
30. Jones S.R., Fernyhough C. Thought as action: inner speech, self-monitoring, and auditory verbal hallucinations. Conscious. Cogn. 2007, 16(2):391-399.
31. Kompus K., Westerhausen R., Hugdahl K. The "paradoxical" engagement of the primary auditory cortex in patients with auditory verbal hallucinations: a meta-analysis of functional neuroimaging studies. Neuropsychologia 2011, 49(12):3361-3369.
32. Lahti A.C., Weiler M.A., Holcomb H.H., Tamminga C.A., Carpenter W.T., McMahon R. Correlations between rCBF and symptoms in two independent cohorts of drug-free patients with schizophrenia. Neuropsychopharmacology 2006, 31(1):221-230.
33. Lennox B.R., Park S.B., Medley I., Morris P.G., Jones P.B. The functional anatomy of auditory hallucinations in schizophrenia. Psychiatry Res. 2000, 100(1):13-20.
34. Liddle P.F., Friston K.J., Frith C.D., Jones T., Hirsch S.R., Frackowiak R.S.J. Patterns of cerebral blood flow in schizophrenia. Br. J. Psychiatry 1992, 160:179-186.
35. Matsuda H., Gyobu T., Hisada K., Ii M. SPECT imaging of auditory hallucination using 123I-IMP. Adv. Funct. Neuroimaging 1989, 2(4):9-16.
36. McCarley R.W., Wible C.G., Frumin M., Hirayasu Y., Levitt J.J., Fischer I.A., Shenton M.E. MRI anatomy of schizophrenia. Biol. Psychiatry 1999, 45:1099-1119.
37. McGuire P.K., Shah G.M., Murray R.M. Increased blood flow in Broca's area during auditory hallucinations in schizophrenia [see comments]. Lancet 1993, 342(8873):703-706.
38. McGuire P.K., Silbersweig D.A., Murray R.M., David A.S., Frackowiak R.S., Frith C.D. Functional anatomy of inner speech and auditory verbal imagery. Psychol. Med. 1996, 26(1):29-38.
39. Mesulam M.-M. Principles of Behavioral and Cognitive Neurology 2000, Oxford University Press, New York, NY. 2nd ed.
40. Modinos G., Costafreda S.G., van Tol M.J., McGuire P.K., Aleman A., Allen P. Neuroanatomy of auditory verbal hallucinations in schizophrenia: a quantitative meta-analysis of voxel-based morphometry studies. Cortex 2012, (Electronic publication ahead of print February 1, 2012).
41. Neckelmann G., Specht K., Lund A., Ersland L., Smievoll A.I., Neckelmann D., Hugdahl K. Mr morphometry analysis of grey matter volume reduction in schizophrenia: association with hallucinations. Int. J. Neurosci. 2006, 116(1):9-23.
42. Northoff G., Qin P. How can the brain's resting state activity generate hallucinations? A 'resting state hypothesis' of auditory verbal hallucinations. Schizophr. Res. 2011, 127(1-3):202-214.
43. Ongur D., Lundy M., Greenhouse I., Shinn A.K., Menon V., Cohen B.M., Renshaw P.F. Default mode network abnormalities in bipolar disorder and schizophrenia. Psychiatry Res. 2010, 183(1):59-68.
44. Pakkenberg B. Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch. Gen. Psychiatry 1990, 47(11):1023-1028.
45. Parellada E., Lomena F., Font M., Pareto D., Gutierrez F., Simo M., Fernandez-Egea E., Pavia J., Ros D., Bernardo M. Fluordeoxyglucose-PET study in first-episode schizophrenic patients during the hallucinatory state, after remission and during linguistic-auditory activation. Nucl. Med. Commun. 2008, 29(10):894-900.
46. Price C.J. The anatomy of language: a review of 100 fMRI studies published in 2009. Ann. N. Y. Acad. Sci. 2010, 1191:62-88.
47. Rademacher J., Morosan P., Schormann T., Schleicher A., Werner C., Freund H.J., Zilles K. Probabilistic mapping and volume measurement of human primary auditory cortex. NeuroImage 2001, 13(4):669-683.
48. Rotarska-Jagiela A., van de Ven V., Oertel-Knochel V., Uhlhaas P.J., Vogeley K., Linden D.E. Resting-state functional network correlates of psychotic symptoms in schizophrenia. Schizophr. Res. 2010, 117(1):21-30.
49. Schoenbaum G., Roesch M.R., Stalnaker T.A., Takahashi Y.K. A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat. Rev. Neurosci. 2009, 10(12):885-892.
50. Seal M.L., Aleman A., McGuire P.K. Compelling imagery, unanticipated speech and deceptive memory: neurocognitive models of auditory verbal hallucinations in schizophrenia. Cogn. Neuropsychiatry 2004, 9(1-2):43-72.
51. 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. Arch. Gen. Psychiatry 2000, 57(11):1033-1038.
52. Silbersweig D.A., Stern E., Frith C., Cahill C., Holmes A., Grootoonk S., Seaward J., McKenna P., Chua S.E., Schnorr L., Jones T., Frackowiak R.S.J. A functional neuroanatomy of hallucinations in schizophrenia. Nature 1995, 378(6553):176-179.
53. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004, 23(Suppl. 1):S208-S219.
54. Sommer I.E., Diederen K.M., Blom J.D., Willems A., Kushan L., Slotema K., Boks M.P., Daalman K., Hoek H.W., Neggers S.F., Kahn R.S. Auditory verbal hallucinations predominantly activate the right inferior frontal area. Brain 2008, 131(Pt. 12):3169-3177.
55. Strauss J.S. Hallucinations and delusions as points on continua function. Rating scale evidence. Arch. Gen. Psychiatry 1969, 21(5):581-586.
56. Suzuki M., Yuasa S., Minabe Y., Murata M., Kurachi M. Left superior temporal blood flow increases in schizophrenic and schizophreniform patients with auditory hallucination: a longitudinal case study using 123I-IMP SPECT. Eur. Arch. Psychiatry Clin. Neurosci. 1993, 242(5):257-261.
57. Sweet R.A., Bergen S.E., Sun Z., Sampson A.R., Pierri J.N., Lewis D.A. Pyramidal cell size reduction in schizophrenia: evidence for involvement of auditory feedforward circuits. Biol. Psychiatry 2004, 55(12):1128-1137.
58. Sweet R.A., Henteleff R.A., Zhang W., Sampson A.R., Lewis D.A. Reduced dendritic spine density in auditory cortex of subjects with schizophrenia. Neuropsychopharmacology 2009, 34(2):374-389.
59. Szechtman H., Woody E., Bowers K.S., Nahmias C. Where the imaginal appears real: a positron emission tomography study of auditory hallucinations. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(4):1956-1960.
60. van de Ven V.G., Formisano E., Roder C.H., Prvulovic D., Bittner R.A., Dietz M.G., Hubl D., Dierks T., Federspiel A., Esposito F., Di Salle F., Jansma B., Goebel R., Linden D.E. The spatiotemporal pattern of auditory cortical responses during verbal hallucinations. NeuroImage 2005, 27(3):644-655.
61. Van Dijk K.R., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 2012, 59(1):431-438.
62. Vercammen A., Knegtering H., den Boer J.A., Liemburg E.J., Aleman A. Auditory hallucinations in schizophrenia are associated with reduced functional connectivity of the temporo-parietal area. Biol. Psychiatry 2010, 67(10):912-918.
63. Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature 2007, 447(7140):83-86.
64. Waters F.A., Badcock J.C., Michie P.T., Maybery M.T. Auditory hallucinations in schizophrenia: intrusive thoughts and forgotten memories. Cogn. Neuropsychiatry 2006, 11(1):65-83.
65. Waters F., Allen P., Aleman A., Fernyhough C., Woodward T.S., Badcock J.C., Barkus E., Johns L., Varese F., Menon M., Vercammen A., Laroi F. Auditory hallucinations in schizophrenia and nonschizophrenia populations: a review and integrated model of cognitive mechanisms. Schizophr. Bull. 2012, 38(4):683-693.
66. Wolf N.D., Sambataro F., Vasic N., Frasch K., Schmid M., Schonfeldt-Lecuona C., Thomann P.A., Wolf R.C. Dysconnectivity of multiple resting-state networks in patients with schizophrenia who have persistent auditory verbal hallucinations. J. Psychiatry Neurosci. 2011, 36(4).
67. Woodruff P.W., Wright I.C., Bullmore E.T., Brammer M., Howard R.J., Williams S.C., Shapleske J., Rossell S., David A.S., McGuire P.K., Murray R.M. Auditory hallucinations and the temporal cortical response to speech in schizophrenia: a functional magnetic resonance imaging study. Am. J. Psychiatry 1997, 154(12):1676-1682.
68. Woolrich M.W., Behrens T.E., Beckmann C.F., Jenkinson M., Smith S.M. Multilevel linear modelling for FMRI group analysis using Bayesian inference. NeuroImage 2004, 21(4):1732-1747.
69. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20(1):45-57.