Auditory Hallucinations in Schizophrenia Are Associated with Reduced Functional Connectivity of the Temporo-Parietal Area

Biological Psychiatry

Volumn 67, Issue 10, 2010, Pages 912-918

  Vercammen, Ans ^a   Knegtering, Henderikus ^a   den Boer, Johann A ^a   Liemburg, Edith J ^a   Aleman, André ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Auditory verbal hallucinations; fMRI; functional connectivity; resting state; schizophrenia; temporo parietal junction

Indexed keywords

ADULT; ARTICLE; AUDITORY HALLUCINATION; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGNOSTIC AND STATISTICAL MANUAL OF MENTAL DISORDERS; DISEASE SEVERITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MENTAL DISEASE; PRIORITY JOURNAL; SCHIZOPHRENIA; SPEECH;

ADULT; FEMALE; HALLUCINATIONS; HUMANS; MALE; NEURAL PATHWAYS; PARIETAL LOBE; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SPEECH PERCEPTION; TEMPORAL LOBE;

EID: 77951620661     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.11.017     Document Type: Article

References (58)

1. Andreasen N.C., and Flaum M. Schizophrenia: The characteristic symptoms. Schizophr Bull 17 (1991) 27-49
2. McGuire P.K., Shah G.M., and Murray R.M. Increased blood flow in Broca's area during auditory hallucinations in schizophrenia. Lancet 342 (1993) 703-706
3. Dierks T., Linden D.E., Jandl M., Formisano E., Goebel R., Lanfermann H., and Singer W. Activation of Heschl's gyrus during auditory hallucinations. Neuron 22 (1999) 615-621
4. Shergill S.S., Brammer M.J., Williams S.C., Murray R.M., and McGuire P.K. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch Gen Psychiatry 57 (2000) 1033-1038
5. Shergill S.S., Brammer M.J., Amaro E., Williams S.C., Murray R.M., and McGuire P.K. Temporal course of auditory hallucinations. Br J Psychiatry 185 (2004) 516-517
6. Hoffman R.E., Anderson A.W., Varanko M., Gore J.C., and Hampson M. Time course of regional brain activation associated with onset of auditory/verbal hallucinations. Br J Psychiatry 193 (2008) 424-425
7. Silbersweig D.A., Stern E., Frith C., Cahill C., Holmes A., Grootoonk S., et al. A functional neuroanatomy of hallucinations in schizophrenia. Nature 378 (1995) 176-179
8. Barta P.E., Pearlson G.D., Powers R.E., Richards S.S., and Tune L.E. Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 147 (1990) 1457-1462
9. Flaum M., O'Leary D.S., Swayze V.W., Miller D.D., Arndt S., and Andreasen N.C. Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders. J Psychiatr Res 29 (1995) 261-276
10. Levitan C., Ward P.B., and Catts S.V. Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia. Biol Psychiatry 46 (1999) 955-962
11. Rajarethinam R.P., DeQuardo J.R., Nalepa R., and Tandon R. Superior temporal gyrus in schizophrenia: A volumetric magnetic resonance imaging study. Schizophr Res 41 (2000) 303-312
12. Onitsuka T., Shenton M.E., Salisbury D.F., Dickey C.C., Kasai K., Toner S.K., et al. Middle and inferior temporal gyrus gray matter volume abnormalities in chronic schizophrenia: An MRI study. Am J Psychiatry 161 (2004) 1603-1611
13. Suzuki M., Yuasa S., Minabe Y., Murata M., and 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 242 (1993) 257-261
14. van de Ven V., Formisano E., Roder C.H., Prvulovic D., Bittner R.A., Dietz M.G., et al. The spatiotemporal pattern of auditory cortical responses during verbal hallucinations. Neuroimage 27 (2005) 644-655
15. Bentaleb L.A., Beauregard M., Liddle P., and Stip E. Cerebral activity associated with auditory verbal hallucinations: A functional magnetic resonance imaging case study. J Psychiatry Neurosci 27 (2002) 110-115
16. Lennox B.R., Park S.B., Medley I., Morris P.G., and Jones P.B. The functional anatomy of auditory hallucinations in schizophrenia. Psychiatry Res 100 (2000) 13-20
17. Lennox B.R., Park S.B., Jones P.B., and Morris P.G. Spatial and temporal mapping of neural activity associated with auditory hallucinations. Lancet 353 (1999) 644
18. Copolov D.L., Seal M.L., Maruff P., Ulusoy R., Wong M.T., Tochon-Danguy H.J., and 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 122 (2003) 139-152
19. Sommer I.E., Diederen K.M., Blom J.D., Willems A., Kushan L., Slotema K., et al. Auditory verbal hallucinations predominantly activate the right inferior frontal area. Brain 131 (2008) 3169-3177
20. Allen P., Laroi F., McGuire P.K., and Aleman A. The hallucinating brain: A review of structural and functional neuroimaging studies of hallucinations. Neurosci Biobehav Rev 32 (2008) 175-191
21. Stephan K.E., Friston K.J., and Frith C.D. Dysconnection in schizophrenia: From abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull 35 (2009) 509-527
22. Zhou Y., Liang M., Tian L., Wang K., Hao Y., Liu H., et al. Functional disintegration in paranoid schizophrenia using resting-state fMRI. Schizophr Res 97 (2007) 194-205
23. Liang M., Zhou Y., Jiang T., Liu Z., Tian L., Liu H., and Hao Y. Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. Neuroreport 17 (2006) 209-213
24. Whitfield-Gabrieli S., Thermenos H.W., Milanovic S., Tsuang M.T., Faraone S.V., McCarley R.W., et al. 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 (2009) 1279-1284
25. Lawrie S.M., Buechel C., Whalley H.C., Frith C.D., Friston K.J., and Johnstone E.C. Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biol Psychiatry 51 (2002) 1008-1011
26. Mechelli A., Allen P., Amaro Jr. E., Fu C.H., Williams S.C., Brammer M.J., et al. Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations. Hum Brain Mapp 28 (2007) 1213-1222
27. Hashimoto R.I., Lee K., Preus A., McCarley R.W., and Wible C.G. An fMRI study of functional abnormalities in the verbal working memory system and the relationship to clinical symptoms in chronic schizophrenia. Cereb Cortex 20 (2010) 46-60
28. Zhou Y., Shu N., Liu Y., Song M., Hao Y., Liu H., et al. Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr Res 100 (2008) 120-132
29. Raichle M.E., and Gusnard D.A. Intrinsic brain activity sets the stage for expression of motivated behavior. J Comp Neurol 493 (2005) 167-176
30. Gusnard D.A., Akbudak E., Shulman G.L., and Raichle M.E. Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc Natl Acad Sci U S A 98 (2001) 4259-4264
31. Gusnard D.A., and Raichle M.E. Searching for a baseline: Functional imaging and the resting human brain. Nat Rev Neurosci 2 (2001) 685-694
32. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., and Shulman G.L. A default mode of brain function. Proc Natl Acad Sci U S A 98 (2001) 676-682
33. Greicius M.D., Krasnow B., Reiss A.L., and Menon V. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 100 (2003) 253-258
34. Fransson P. Spontaneous low-frequency BOLD signal fluctuations: An fMRI investigation of the resting-state default mode of brain function hypothesis. Hum Brain Mapp 26 (2005) 15-29
35. Hoffman R.E., Hampson M., Wu K., Anderson A.W., Gore J.C., Buchanan R.J., et al. Probing the pathophysiology of auditory/verbal hallucinations by combining functional magnetic resonance imaging and transcranial magnetic stimulation. Cereb Cortex 17 (2007) 2733-2743
36. Giel R., and Nienhuis F.J. SCAN-2.1: Schedules for Clinical Assessment in Neuropsychiatry. [trans] (1996), World Health Organization, Geneva/Groningen
37. Hoffman R.E., Hawkins K.A., Gueorguieva R., Boutros N.N., Rachid F., Carroll K., and Krystal J.H. Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch Gen Psychiatry 60 (2003) 49-56
38. Kay S.R., Fiszbein A., and Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13 (1987) 261-276
39. Fox P.T., and Lancaster J.L. Neuroscience on the net. Science 266 (1994) 994-996
40. Nielsen F.A., and Hansen L.K. Modeling of activation data in the BrainMap database: Detection of outliers. Hum Brain Mapp 15 (2002) 146-156
41. Benjamini Y., and Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc 57 (1995) 289-300
42. Thiel A., Schumacher B., Wienhard K., Gairing S., Kracht L.W., Wagner R., et al. Direct demonstration of transcallosal disinhibition in language networks. J Cereb Blood Flow Metab 26 (2006) 1122-1127
43. Voets N.L., Adcock J.E., Flitney D.E., Behrens T.E., Hart Y., Stacey R., et al. Distinct right frontal lobe activation in language processing following left hemisphere injury. Brain 129 (2006) 754-766
44. Van Lancker D. Rags to riches: Our increasing appreciation of cognitive and communicative abilities of the human right hemisphere. Brain Lang 57 (1997) 1-11
45. Van Lancker D., and Cummings J.L. Expletives: Neurolinguistic and neurobehavioral perspectives on swearing. Brain Res Brain Res Rev 31 (1999) 83-104
46. Shergill S.S., Tracy D.K., Seal M., Rubia K., and McGuire P. Timing of covert articulation: An fMRI study. Neuropsychologia 44 (2006) 2573-2577
47. Ford J.M., and Mathalon D.H. Electrophysiological evidence of corollary discharge dysfunction in schizophrenia during talking and thinking. J Psychiatr Res 38 (2004) 37-46
48. Ford J.M., Roach B.J., Faustman W.O., and Mathalon D.H. Synch before you speak: Auditory hallucinations in schizophrenia. Am J Psychiatry 164 (2007) 458-466
49. Ford J.M., Mathalon D.H., Whitfield S., Faustman W.O., and Roth W.T. Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biol Psychiatry 51 (2002) 485-492
50. 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. Am J Psychiatry 164 (2007) 467-473
51. Dosenbach N.U., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A., et al. Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci U S A 104 (2007) 11073-11078
52. Craig A.D. Disembodied hallucinatory voices:Comment on Sommer, et al., 2008. Brain 131 (2009) 3169-3177
53. Aleman A., and Kahn R.S. Strange feelings: Do amygdala abnormalities dysregulate the emotional brain in schizophrenia?. Prog Neurobiol 77 (2005) 283-298
54. Sanjuan J., Lull J.J., Aguilar E.J., Marti-Bonmati L., Moratal D., Gonzalez J.C., et al. Emotional words induce enhanced brain activity in schizophrenic patients with auditory hallucinations. Psychiatry Res 154 (2007) 21-29
55. Kapur S. Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry 160 (2003) 13-23
56. Sander D., Grafman J., and Zalla T. The human amygdala: An evolved system for relevance detection. Rev Neurosci 14 (2003) 303-316
57. Kim J.W., Choi E.A., Kim J.J., Jeong B.S., Kim S.E., and Ki S.W. The role of amygdala during auditory verbal imagery of derogatory appraisals by others. Neurosci Lett 446 (2008) 1-6
58. Nielsen F.Å., and Hansen L.K. Automatic anatomical labeling of Talairach coordinates and generation of volumes of interest via the BrainMap database (June 2-6, 2002), NeuroImage, Sendai, Japan [CD-ROM] 16