Advertisement
Original article| Volume 49, ISSUE 8, P685-693, April 15, 2001

Download started.

Ok

Are auditory hallucinations the consequence of abnormal cerebral lateralization? A morphometric MRI study of the sylvian fissure and planum temporale

      Abstract

      Background: Auditory verbal hallucinations (AVHs) are a characteristic feature of schizophrenia. Patients with schizophrenia have been found to have reduced volumes of a variety of brain structures as well as a reduction in right–left asymmetries, using postmortem and magnetic resonance imaging (MRI) measures. There is also evidence that patients with AVHs differ in these structural asymmetries, relative to those patients who do not hallucinate. The aim of this study was to examine whether patients with and without a prominent history of AVHs differ, both from each other and in comparison with normal subjects, in the asymmetry of the sylvian fissure (SF) and planum temporale (PT).
      Methods: We recruited 74 DSM-IV male patients with schizophrenia (on the basis of their AVH history) and 32 matched normal control subjects. Thirty patients had no history of AVHs and 44 had a strong definitive history of AVHs. The SF length and PT area and volume were measured on a three-dimensional MRI spoiled GRASS volume sequence. Absolute measures and laterality coefficients were calculated.
      Results: All groups had the normal leftward asymmetry in both the SF and PT. Planum temporale volume and surface area and SF length were all larger in the left hemisphere. There were no significant differences in any measures between the two patient groups or between schizophrenic patients and control subjects. Greater leftward asymmetry of the SF correlated with hallucinations and thought disorder within the prominent hallucinator group. An association was found between handedness and brain size, but this did not interact with diagnosis.
      Conclusions: The results of this study do not confirm reports, based on smaller samples, of reduced structural asymmetries of either the SF or PT in schizophrenia, nor do they indicate a specific relationship to a propensity to experience AVHs. A modest correlation between leftward asymmetry of the SF and some positive symptomatology was found.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Barta P.E
        • Pearlson G.D
        • Brill L.B
        • et al.
        Planum temporale asymmetry reversal in schizophrenia.
        Am J Psychiatry. 1997; 154: 611-667
        • Barta P.E
        • Pearlson G.D
        • Powers R.E
        • et al.
        Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia.
        Am J Psychiatry. 1990; 147: 457-462
        • Barta P.E
        • Petty R.G
        • McGilchrist I
        • Lewis R.W
        • Jerram M
        • Casanova M.F
        • et al.
        Asymmetry of the planum temporale.
        Psychiatry Res: Neuroimaging. 1995; 61: 137-150
        • Bartley A.J
        • Jones D.W
        • Torrey-Fuller E
        • et al.
        Sylvian fissure asymmetry in monozygotic twins.
        Biol Psychiatry. 1993; 34: 853-865
        • Beaton A.A
        The relation of planum temporale asymmetry and morphology of the corpus callosum to handedness, gender, and dyslexia.
        Brain Lang. 1997; 60: 255-322
        • Bilder R.M
        • Wu H
        • Bogerts B
        • et al.
        Absence of regional hemispheric volume asymmetries in first-episode schizophrenia.
        Am J Psychiatry. 1994; 151: 1437-1447
        • Cunningham D.J
        Cunningham Memoires No. VII. Royal Irish Academy, Dublin1892
        • David A
        • Woodruff P.W.R
        • Howard R
        • et al.
        Auditory hallucinations inhibit exogenous activation of auditory association cortex.
        Neuroreport. 1996; 7: 932-936
        • David A.S
        The neuropsychology of auditory-verbal hallucinations.
        in: David A Cutting J The Neuropsychology of Schizophrenia. Erlbaum, Hove, UK1994: 269-312
        • David A.S
        • Busatto G
        The hallucination.
        in: Ron M.A David A.S Disorders of Brain and Mind. Cambridge University Press, Cambridge, UK1998: 336-362
        • DeLisi L.E
        • Hoff A.L
        • Neale C
        • Kushner M
        Asymmetry in the superior temporal lobe in men and women first schizophrenic patients. Measure of the planum temporal and superior temporal gyrus in MRI.
        Schizophr Res. 1994; 12: 19-28
        • Dierks T
        • Linden D.E.J
        • Jandl M
        • et al.
        Activation of Heschl’s gyrus during auditory hallucinations.
        Neuron. 1999; 22: 615-621
        • Eberstaller O
        Das Stirnhirn. Urban and Schwarzenberg, Vienna1890
        • Falkai P
        • Bogerts B
        • Greve B
        • et al.
        Loss of Sylvian fissure asymmetry in schizophrenia.
        Schizophr Res. 1992; 7: 23-32
        • Falkai P
        • Bogerts B
        • Schneider T
        • et al.
        Disturbed planum temporale asymmetry in schizophrenia. A quantitative post-mortem study.
        Schizophr Res. 1995; 14: 161-176
        • Flaum M
        • O’Leary D.S
        • Swayze V.W
        • et al.
        Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders.
        J Psychiatr Res. 1995; 29: 261-276
        • Frangou S
        • Sharma T
        • Sigmundsson T
        • et al.
        The Maudsley Family Study 4. Normal planum temporale asymmetry in familial schizophrenia.
        Br J Psychiatry. 1997; 170: 328-333
        • Gaser C
        • Volz H.P
        • Kiebel S
        • et al.
        Detecting structural changes in whole brain based on nonlinear deformations—application to schizophrenia research.
        Neuroimage. 1999; 10: 107-113
        • Habib M
        • Robichon F
        • Lerier O
        • et al.
        Diverging asymmetries of temporo-parietal cortical areas.
        Brain Lang. 1995; 12: 238-258
        • Hoff A.L
        • Riodon H
        • O’Donnell D
        • et al.
        Anomalous lateral sulcus asymmetry dysfunction in first episode schizophrenia.
        Schizophr Bull. 1992; 18: 257-272
        • Holinger D.P
        • Shenton M.E
        • Wible C.G
        • et al.
        Superior temporal gyrus volume abnormalities and thought disorder in left-handed schizophrenic men.
        Am J Psychiatry. 1999; 156: 1730-1735
        • Kulynych J.J
        • Vladar K
        • Jones D.W
        • Weinberger A
        A 3D surface rendering in MRI morphometry.
        J Comput Assist Tomogr. 1993; 17: 529-535
        • Kwon J.S
        • McCarley R.W
        • Hirayasu Y
        • et al.
        Left planum temporale volume reduction in schizophrenia.
        Arch Gen Psychiatry. 1999; 56: 142-148
        • Lennox B.R
        • Bert S
        • Park B.G
        • et al.
        Spatial and temporal mapping of neural activity associated with auditory hallucinations.
        Lancet. 1999; 353: 644
        • Levitan C
        • Ward P.B
        • Catts S.V
        Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia.
        Biol Psychiatry. 1999; 46: 955-962
        • Luchins D.J
        • Weinberger D.R
        • Wyatt R.J
        Schizophrenia.
        Arch Gen Psychiatry. 1979; 36: 1309-1311
        • McCarley R.W
        • Shenton M.E
        • O’Donnell B.F
        • et al.
        Auditory P300 abnormalities and left posterior superior temporal gyrus volume reduction in schizophrenia.
        Arch Gen Psychiatry. 1993; 50: 190-197
        • McCarley R.W
        • Wible C.G
        • Frumin M
        • et al.
        MRI anatomy of schizophrenia.
        Biol Psychiatry. 1999; 45: 1099-1119
        • Menon R.J
        • Barta P.E
        • Aylward E.H
        • et al.
        Posterior superior temporal gyrus in schizophrenia.
        Schizophr Res. 1995; 16: 127-135
        • Moffat S.D
        • Hampson E
        • Lee D.H
        Morphology of the planum temporale and corpus callosum in left handers with evidence of left and right hemisphere speech representation.
        Brain. 1998; 121: 2369-2379
        • Naeser M.A
        • Levine H.L
        • Benson D.F
        • et al.
        Frontal leukotomy size and hemispheric asymmetries on computerized tomographic scans of schizophrenics with variable recovery.
        Arch Neurol. 1981; 38: 30-37
        • Nayani T.H
        • David A.S
        The auditory hallucination.
        Psychol Med. 1996; 26: 177-189
        • Petty R.G
        • Barta P.E
        • Pearlson G.D
        • et al.
        Reversal of asymmetry of the planum temporale in schizophrenia.
        Am J Psychiatry. 1995; 152: 715-721
        • Reitan R.M
        • Wolfson D
        The Halstead-Reitan Neuropsychological Test Battery.
        in: Wedding D Horton Jr, A.M The Neuropsychology Handbook Behavioral and Clinical Perspectives. Springer, New York1986: 134-160
      1. Rossell SL, Shapleske J, Fukuda R, et al (2000): Corpus callosum area and functioning in schizophrenic patients with auditory-verbal hallucinations. Schizophr Res.

        • Rossi A
        • Serio A
        • Stratta P
        • et al.
        3D in vivo planum temporale reconstruction.
        Brain Lang. 1994; 47: 89-95
        • Shapleske J
        • Rossell S.L
        • Woodruff P.W.R
        • David A.S
        The planum temporale.
        Brain Res Rev. 1999; 29: 26-49
        • Shellshear J.L
        The brain of the Aboriginal Australian.
        Philos Trans R Soc Lond B Biol Sci. 1937; 227: 293-409
        • Shenton M.E
        • Kikinis R
        • Jolesz F.A
        • et al.
        Abnormalities of the left temporal lobe and thought disorder in schizophrenia.
        N Engl J Med. 1992; 327: 604-612
        • Simmons A
        • Arridge S.R
        • Barker G.J
        • Williams S.C.R
        Simulation of MRI cluster plots and application to neurological segmentation.
        Magn Reson Imaging. 1996; 14: 73-92
        • Steinmetz H
        • Volkman J
        • Janche L
        • Freund H
        Anatomical asymmetry of language related temporal cortex in left and right handers.
        Ann Neurol. 1991; 29: 315-319
        • Suckling J
        • Brammer M.J
        • Lingford-Hughes A
        • Bullmore E.T
        Removal of extracortical tissues in dual-echo magnetic resonance images via linear scale space features.
        Magn Reson Imaging. 1999; 17: 247-256
        • Suckling J
        • Sigmundsson T
        • Greenwood K
        • Bullmore E.T
        A refined fuzzy clustering algorithm for operator independent brain tissue classification of dual echo MR images.
        Magn Reson Imaging. 1999; 17: 1065-1076
        • Suddath R.L
        • Casanova M.F
        • Goldberg T.E
        • et al.
        Temporal lobe pathology in schizophrenia.
        Am J Psychiatry. 1989; 146: 464-472
        • Suzuki M
        • Yuasa S
        • Minabe Y
        • et al.
        Left superior temporal blood flow increases in schizophrenic and schizophreniform patients with auditory hallucinations.
        Eur Arch Psychiatr Clin Neurosci. 1993; 242: 257-261
        • Tsai L
        • Nasrallah H.A
        • Jacoby C.G
        Hemispheric asymmetries on computed tomographic scans in schizophrenia and mania.
        Arch Gen Psychiatry. 1983; 40: 1286-1289
        • Vita A
        • Dieci M
        • Giobbio G.M
        • et al.
        Language and thought disorder in schizophrenia.
        Schizophr Res. 1995; 15: 243-251
        • Witelson S.F
        • Kigar D.L
        Sylvian fissure morphology and asymmetry in men and women.
        J Comp Neurol. 1992; 323: 326-340
        • Woodruff P
        • Brammer M
        • Mellers J
        • Wright I
        • Bullmore E
        • Williams S
        Auditory hallucinations and perception of external speech.
        Lancet. 1995; 346: 1035
        • Woodruff P.W.R
        • Wright I.C
        • Bullmore E.T
        • et al.
        Auditory hallucinations and the temporal cortical response to speech in schizophrenia.
        Am J Psychiatry. 1997; 154: 1676-1682
      2. Wright IC, Rabe-Hesketh S, Woodruff PWR, et al (in press): Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157:16–25.

      Linked Article