Background/Aims: Heschl’s gyrus (HG) is functionally involved in the genesis of auditory verbal hallucinations (AVH). This dysfunction seems to be structurally facilitated. The aim of the study was to analyze macrostructural features of HG in a group of patients reporting AVH who demonstrated white matter diffusion tensor imaging abnormalities reported previously. Methods: 3-D anatomical MR scans were obtained (patients with and without history of AVH, controls). HG was delineated by manual segmentation. Cortical folding, absolute and relative volumes, laterality were analyzed. Results: According to the literature, in the collapsed group of patients, the normal left-greater-than-right laterality of HG was attenuated. We found a trend towards a higher number of duplicated HG in hallucinating patients. We also found a bigger volume of HG in the right hemisphere in hallucinating patients. This effect was caused by gray and white matter increase. Conclusions: This is the first study on manual volumetry of HG in a group of schizophrenia patients with AVH compared to patients without AVH. In a previous analysis of the diffusion tensor imaging data of the here presented sample, we found higher directionality of the arcuate fasciculus in patients with AVH, facilitating abnormal co-activation in the auditory cortices in the hallucinating brain. As these abnormal activations are frequent in hallucinating patients, the here described volume increase of HG might be interpreted as compensatory plastic adaptations of the contralateral regions. We suggest that this volume increase of HG is caused by the symptomatology and not by the underlying disorder of schizophrenia.
© 2009 S. Karger AG, Basel
- Auditory verbal hallucinations
- Heschl’s gyrus
- Magnetic resonance imaging
- Schneider K: Klinische Psychopathologie, ed 15. Stuttgart, Thieme, 2007.
- David AS: The cognitive neuropsychiatry of auditory verbal hallucinations: an overview. Cognit Neuropsychiatry 2004;9:107–123.
- Crow TJ: Is schizophrenia the price that Homo sapiens pays for language? Schizophr Res 1997;28:127–141.
- Dierks T, Linden DE, Jandl M, Formisano E, Goebel R, Lanfermann H, Singer W: Activation of Heschl’s gyrus during auditory hallucinations. Neuron 1999;22:615–621.
- McGuire PK, Shah GM, Murray RM: Increased blood flow in Broca’s area during auditory hallucinations in schizophrenia. Lancet 1993;342:703–706.
- Shergill SS, Brammer MJ, Williams SC, Murray RM, McGuire PK: Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch Gen Psychiatry 2000;57:1033–1038.
- Hubl D, Koenig T, Strik WK, Garcia LM, Dierks T: Competition for neuronal resources: how hallucinations make themselves heard. Br J Psychiatry 2007;190:57–62.
- Hubl D, Koenig T, Strik W, Federspiel A, Kreis R, Boesch C, Maier SE, Schroth G, Lovblad K, Dierks T: Pathways that make voices: white matter changes in auditory hallucinations. Arch Gen Psychiatry 2004;61:658–668.
- Allen P, Laroi F, McGuire PK, Aleman A: The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci Biobehav Rev 2008;32:175–191.
- Shapleske J, Rossell SL, Woodruff PW, David AS: The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Brain Res Rev 1999;29:26–49.
- Zetzsche T, Meisenzahl EM, Preuss UW, Holder JJ, Kathmann N, Leinsinger G, Hahn K, Hegerl U, Moller HJ: In-vivo analysis of the human planum temporale (PT): does the definition of PT borders influence the results with regard to cerebral asymmetry and correlation with handedness? Psychiatry Res 2001;107:99–115.
- Meisenzahl EM, Zetzsche T, Preuss U, Frodl T, Leinsinger G, Moller HJ: Does the definition of borders of the planum temporale influence the results in schizophrenia? Am J Psychiatry 2002;159:1198–1200.
- Rajarethinam RP, DeQuardo JR, Nalepa R, Tandon R: Superior temporal gyrus in schizophrenia: a volumetric magnetic resonance imaging study. Schizophr Res 2000;41:303–312.
- Crespo-Facorro B, Kim JJ, Chemerinski E, Magnotta V, Andreasen NC, Nopoulos P: Morphometry of the superior temporal plane in schizophrenia: relationship to clinical correlates. J Neuropsychiatry Clin Neurosci 2004;16:284–294.
- Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE: Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry 1990;147:1457–1462.
- Levitan C, Ward PB, Catts SV: Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia. Biol Psychiatry 1999;46:955–962.
- Flaum M, O’Leary DS, Swayze VW, Miller DD, Arndt S, Andreasen NC: Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders. J Psychiatr Res 1995;29:261–276.
- DeLisi LE, Hoff AL, Neale C, Kushner M: Asymmetries in the superior temporal lobe in male and female first-episode schizophrenic patients: measures of the planum temporale and superior temporal gyrus by MRI. Schizophr Res 1994;12:19–28.
- Cowell PE, Kostianovsky DJ, Gur RC, Turetsky BI, Gur RE: Sex differences in neuroanatomical and clinical correlations in schizophrenia. Am J Psychiatry 1996;153:799–805.
- Shapleske J, Rossell SL, Simmons A, David AS, Woodruff PW: Are auditory hallucinations the consequence of abnormal cerebral lateralization? A morphometric MRI study of the sylvian fissure and planum temporale. Biol Psychiatry 2001;49:685–693.
- Havermans R, Honig A, Vuurman EF, Krabbendam L, Wilmink J, Lamers T, Verheecke CJ, Jolles J, Romme MA, van Praag HM: A controlled study of temporal lobe structure volumes and P300 responses in schizophrenic patients with persistent auditory hallucinations. Schizophr Res 1999;38:151–158.
- Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Onitsuka T, Spencer MH, Yurgelun-Todd DA, Kikinis R, Jolesz FA, McCarley RW: Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 2003;60:766–775.
- Salisbury DF, Kuroki N, Kasai K, Shenton ME, McCarley RW: Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia. Arch Gen Psychiatry 2007;64:521–529.
- Shergill SS, Kanaan RA, Chitnis XA, O’Daly O, Jones DK, Frangou S, Williams SC, Howard RJ, Barker GJ, Murray RM, McGuire P: A diffusion tensor imaging study of fasciculi in schizophrenia. Am J Psychiatry 2007;164:467–473.
- Rotarska-Jagiela A: Anatomical brain connectivity and positive symptoms of schizophrenia: a diffusion tensor imaging study. Psychiatry Res 2009 (in press).
- Golestani N, Pallier C: Anatomical correlates of foreign speech sound production. Cereb Cortex 2007;17:929–934.
- Van Praag H, Kempermann G, Gage FH: Neural consequences of environmental enrichment. Nat Rev Neurosci 2000;1:191–198.
- Schneider P, Scherg M, Dosch HG, Specht HJ, Gutschalk A, Rupp A: Morphology of Heschl’s gyrus reflects enhanced activation in the auditory cortex of musicians. Nat Neurosci 2002;5:688–694.
- Kay SR, Fiszbein A, Opler LA: The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 1987;13:261–276.
- National Institute for Mental Health. 12 – CGI. Clinical Global Impressions; in Guy W, Bonato R (eds): Manual for the ECDEU Assessment Battery, ed 2 rev. Maryland, Chevy Chase, 1970.
- Pfeifer RA: Myelogenetisch-anatomische Untersuchungen über das Kortikale Ende der Hörleitung. Leipzig, Teubner, 1920.
- Yousry TA: Heschl’s gyrus. Int J Neuroradiol 1997;3:2–12.
- Kwon JS, McCarley RW, Hirayasu Y, Anderson JE, Fischer IA, Kikinis R, Jolesz FA, Shenton ME: Left planum temporale volume reduction in schizophrenia. Arch Gen Psychiatry 1999;56:142–148.
- Hirayasu Y, McCarley RW, Salisbury DF, Tanaka S, Kwon JS, Frumin M, Snyderman D, Yurgelun-Todd D, Kikinis R, Jolesz FA, Shenton ME: Planum temporale and Heschl gyrus volume reduction in schizophrenia: a magnetic resonance imaging study of first-episode patients. Arch Gen Psychiatry 2000;57:692–699.
- Price CJ, Crinion J: The latest on functional imaging studies of aphasic stroke. Curr Opin Neurol 2005;18:429–434.
- Cao Y, Vikingstad EM, George KP, Johnson AF, Welch KM: Cortical language activation in stroke patients recovering from aphasia with functional MRI. Stroke 1999;30:2331–2340.
- Andoh J, Martinot JL: Interhemispheric compensation: a hypothesis of TMS-induced effects on language-related areas. Eur Psychiatry 2008;23:281–288.
- Horn H, Federspiel A, Wirth M, Muller TJ, Wiest R, Wang JJ, Strik W: Structural and metabolic changes in language areas linked to formal thought disorder. Br J Psychiatry 2009;194:130–138.
- Strik WK, Dierks T, Franzek E, Stober G, Maurer K: P300 asymmetries in schizophrenia revisited with reference-independent methods. Psychiatry Res 1994;55:153–166.
- Shenton ME, Dickey CC, Frumin M, McCarley RW: A review of MRI findings in schizophrenia. Schizophr Res 2001;49:1–52.
- McCarley RW, Nakamura M, Shenton ME, Salisbury DF: Combining ERP and structural MRI information in first episode schizophrenia and bipolar disorder. Clin EEG Neurosci 2008;39:57–60.
- Angrilli A, Spironelli C, Elbert T, Crow TJ, Marano G, Stegagno L: Schizophrenia as failure of left hemispheric dominance for the phonological component of language. PLoS ONE 2009;4:e4507.
- Mitchell RL, Crow TJ: Right hemisphere language functions and schizophrenia: the forgotten hemisphere? Brain 2005;128:963–978.
- Paus T, Zijdenbos A, Worsley K, Collins DL, Blumenthal J, Giedd JN, Rapoport JL, Evans AC: Structural maturation of neural pathways in children and adolescents: in vivo study. Science 1999;283:1908–1911.
- Cachia A, Paillère-Martinot ML, Galinow-ski A, Januel D, de Beaurepaire R, Bellivier F, Artiges E, Andoh J, Bartrés-Faz D, Duchesnay E, Rivière D, Plaze M, Mangin JF, Martinot JL: Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations. Neuroimage 2008;39:927–935.
- Shin SE, Lee JS, Kang MH, Kim CE, Bae JN, Jung G: Segmented volumes of cerebrum and cerebellum in first episode schizophrenia with auditory hallucinations. Psychiatry Res 2005;138:33–42.
- Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullen F: Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 2005;8:1148–1150.
- Dickey CC, McCarley RW, Voglmaier MM, Frumin M, Niznikiewicz MA, Hirayasu Y, Fraone S, Seidman LJ, Shenton ME: Smaller left Heschl’s gyrus volume in patients with schizotypal personality disorder. Am J Psychiatry 2002;159:1521–1527.
- Penhune VB, Zatorre RJ, MacDonald JD, Evans AC: Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex 1996;6:661–672.
- McCarley RW, Salisbury DF, Hirayasu Y, Yurgelun-Todd DA, Tohen M, Zarate C, Kikinis R, Jolesz FA, Shenton ME: Association between smaller left posterior superior temporal gyrus volume on magnetic resonance imaging and smaller left temporal P300 amplitude in first-episode schizophrenia. Arch Gen Psychiatry 2002;59:321–331.
Daniela Hubl, MD
University Hospital of Clinical Psychiatry
Bolligenstrasse 111, CH–3000 Bern 60 (Switzerland)
Tel. +41 31 930 9522, Fax +41 31 930 9404
Received: October 10, 2008
Accepted after revision: May 20, 2009
Published online: November 13, 2009
Number of Print Pages : 9
Number of Figures : 3, Number of Tables : 4, Number of References : 50
Additional supplementary material is available online - Number of Parts : 1
Neuropsychobiology (International Journal of Experimental and Clinical Research in Biological Psychiatry, Pharmacopsychiatry, Biological Psychology/Pharmacopsychology and Pharmacoelectroencephalography)
Vol. 61, No. 1, Year 2010 (Cover Date: December 2009)
Journal Editor: Strik W. (Bern)
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