Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-28T15:21:05.022Z Has data issue: false hasContentIssue false
  • English
  • Français

Auditory verbal hallucinations are related to cortical thinning in the left middle temporal gyrus of patients with schizophrenia

Published online by Cambridge University Press:  19 June 2017

Y. Cui ,
B. Liu ,
M. Song ,
D. M. Lipnicki ,
J. Li ,
S. Xie ,
Y. Chen ,
P. Li ,
L. Lu  and
L. Lv
...Show all authors
Y. Cui
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, China University of Chinese Academy of Sciences, Beijing, China
B. Liu
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, China University of Chinese Academy of Sciences, Beijing, China CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Automation, Chinese Academy of Sciences, Beijing, China
M. Song
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, China University of Chinese Academy of Sciences, Beijing, China
D. M. Lipnicki
Affiliation:
CHeBA (Centre for Healthy Brain Ageing), School of Psychiatry, University of New South Wales, Randwick, NSW, Australia
J. Li
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, China University of Chinese Academy of Sciences, Beijing, China
S. Xie
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, China University of Chinese Academy of Sciences, Beijing, China
Y. Chen
Affiliation:
Department of Psychiatry, Xijing Hospital, The Fourth Military Medical University, Xi'an, China
P. Li
Affiliation:
Peking University Sixth Hospital/Institute of Mental Health, Beijing, China Key Laboratory of Mental Health, Ministry of Health (Peking University), Beijing, China
L. Lu
Affiliation:
Peking University Sixth Hospital/Institute of Mental Health, Beijing, China Key Laboratory of Mental Health, Ministry of Health (Peking University), Beijing, China Center for Life Sciences/PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing, China
L. Lv
Affiliation:
Department of Psychiatry, Henan Mental Hospital, The Second Affiliated Hospital of Xinxiang Medical University, Xinxiang, China Henan Key Lab of Biological Psychiatry, Xinxiang Medical University, Xinxiang, China
H. Wang
Affiliation:
Department of Psychiatry, Xijing Hospital, The Fourth Military Medical University, Xi'an, China
H. Yan
Affiliation:
Peking University Sixth Hospital/Institute of Mental Health, Beijing, China Key Laboratory of Mental Health, Ministry of Health (Peking University), Beijing, China
J. Yan
Affiliation:
Peking University Sixth Hospital/Institute of Mental Health, Beijing, China Key Laboratory of Mental Health, Ministry of Health (Peking University), Beijing, China
H. Zhang
Affiliation:
Department of Psychiatry, Henan Mental Hospital, The Second Affiliated Hospital of Xinxiang Medical University, Xinxiang, China Henan Key Lab of Biological Psychiatry, Xinxiang Medical University, Xinxiang, China Department of Psychology, Xinxiang Medical University, Xinxiang, China
D. Zhang
Affiliation:
Peking University Sixth Hospital/Institute of Mental Health, Beijing, China Key Laboratory of Mental Health, Ministry of Health (Peking University), Beijing, China Center for Life Sciences/PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing, China
T. Jiang*
Affiliation:
Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing, China National Laboratory of Pattern Recognition, Institute of Automation, Chinese Academy of Sciences, Beijing, China University of Chinese Academy of Sciences, Beijing, China CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Automation, Chinese Academy of Sciences, Beijing, China Key Laboratory for NeuroInformation of Ministry of Education, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu, China Queensland Brain Institute, University of Queensland, Brisbane, QLD, Australia
*
*Address for correspondence: Tianzi Jiang, Ph.D., Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, China. (Email: jiangtz@nlpr.ia.ac.cn)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Auditory verbal hallucinations (AVHs) are one of the most common and severe symptoms of schizophrenia, but the neuroanatomical abnormalities underlying AVHs are not well understood. The present study aims to investigate whether AVHs are associated with cortical thinning.

Methods

Participants were schizophrenia patients from four centers across China, 115 with AVHs and 93 without AVHs, as well as 261 healthy controls. All received 3 T T1-weighted brain scans, and whole brain vertex-wise cortical thickness was compared across groups. Correlations between AVH severity and cortical thickness were also determined.

Results

The left middle part of the middle temporal gyrus (MTG) was significantly thinner in schizophrenia patients with AVHs than in patients without AVHs and healthy controls. Inferences were made using a false discovery rate approach with a threshold at p < 0.05. Left MTG thickness did not differ between patients without AVHs and controls. These results were replicated by a meta-analysis showing them to be consistent across the four centers. Cortical thickness of the left MTG was also found to be inversely correlated with hallucination severity across all schizophrenia patients.

Conclusion

The results of this multi-center study suggest that an abnormally thin left MTG could be involved in the pathogenesis of AVHs in schizophrenia.

Keywords

Auditory verbal hallucinationcortical thicknessmagnetic resonance imagingmiddle temporal gyrusschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 1 , January 2018 , pp. 115 - 122
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, P, Larøi, F, McGuire, PK, Aleman, A (2008). The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neuroscience & Biobehavioral Reviews 32, 175–191.CrossRefGoogle Scholar
Andreasen, NC, Flaum, M (1991). Schizophrenia: the characteristic symptoms. Schizophrenia Bulletin 17, 27–49.Google Scholar
Barta, PE, Pearlson, GD, Powers, RE, Richards, SS, Tune, LE (1990). Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. American Journal of Psychiatry 147, 1457–1462.Google ScholarPubMed
Benetti, S, Pettersson-Yeo, W, Allen, P, Catani, M, Williams, S, Barsaglini, A, Kambeitz-Ilankovic, LM, McGuire, P, Mechelli, A (2015). Auditory verbal hallucinations and brain dysconnectivity in the perisylvian language network: a multimodal investigation. Schizophrenia Bulletin 41, 192–200.CrossRefGoogle ScholarPubMed
Binney, RJ, Parker, GJ, Ralph, MAL (2012). Convergent connectivity and graded specialization in the rostral human temporal lobe as revealed by diffusion-weighted imaging probabilistic tractography. Journal of Cognitive Neuroscience 24, 1998–2014.Google Scholar
Cabeza, R, Nyberg, L (2000). Imaging cognition II: an empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience 12, 1–47.Google Scholar
Catani, M, ffytche, DH (2005). The rises and falls of disconnection syndromes. Brain 128, 2224–2239.CrossRefGoogle ScholarPubMed
Chen, X, Liang, S, Pu, W, Song, Y, Mwansisya, TE, Yang, Q, Liu, H, Liu, Z, Shan, B, Xue, Z (2015). Reduced cortical thickness in right Heschl's gyrus associated with auditory verbal hallucinations severity in first-episode schizophrenia. BMC Psychiatry 15, 152.Google Scholar
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179–194.Google Scholar
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences 97, 11050–11055.Google Scholar
Fischl, B, Sereno, MI, Dale, AM (1999). Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195–207.CrossRefGoogle Scholar
Flaum, M, O'Leary, DS, Swayze, VW, Miller, DD, Arndt, S, Andreasen, NC (1995). Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders. Journal of Psychiatric Research 29, 261–276.Google Scholar
Frith, CD, Done, DJ (1988). Towards a neuropsychology of schizophrenia. British Journal of Psychiatry 153, 437–443.CrossRefGoogle ScholarPubMed
Garrison, JR, Fernyhough, C, McCarthy-Jones, S, Haggard, M, Australian Schizophrenia Research Bank, Simons, JS (2015). Paracingulate sulcus morphology is associated with hallucinations in the human brain. Nature Communications 6, 8956.Google Scholar
Giraud, AL, Kell, C, Thierfelder, C, Sterzer, P, Russ, MO, Preibisch, C, Kleinschmidt, A (2004). Contributions of sensory input, auditory search and verbal comprehension to cortical activity during speech processing. Cerebral Cortex 14, 247–255.Google Scholar
Glasser, MF, Rilling, JK (2008). DTI tractography of the human brain's language pathways. Cerebral Cortex 18, 2471–2482.Google Scholar
Gogtay, N, Giedd, JN, Lusk, L, Hayashi, KM, Greenstein, D, Vaituzis, AC, Nugent, TF, Herman, DH, Clasen, LS, Toga, AW, Rapoport, JL, Thompson, PM (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences 101, 8174–8179.CrossRefGoogle ScholarPubMed
Goldman, AL, Pezawas, L, Mattay, VS, Fischl, B, Verchinski, BA, Chen, Q, Weinberger, DR, Meyer-Lindenberg, A (2009). Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Archives of General Psychiatry 66, 467–477.CrossRefGoogle ScholarPubMed
Hoffman, RE (2008). Auditory/verbal hallucinations, speech perception neurocircuitry, and the social deafferentation hypothesis. Clinical EEG and Neuroscience 39, 87–90.CrossRefGoogle ScholarPubMed
Hoffman, RE, Hawkins, KA, Gueorguieva, R, Boutros, NN, Rachid, F, Carroll, K, Krystal, JH (2003). Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Archives of General Psychiatry 60, 49–56.CrossRefGoogle ScholarPubMed
Jardri, R, Pouchet, A, Pins, D, Thomas, P (2011). Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. American Journal of Psychiatry 168, 73–81.Google Scholar
Karnath, HO (2001). New insights into the functions of the superior temporal cortex. Nature Reviews Neuroscience 2, 568–576.CrossRefGoogle ScholarPubMed
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.Google Scholar
Lennox, BR, Park, SB, Jones, PB, Morris, PG (1999). Spatial and temporal mapping of neural activity associated with auditory hallucinations. Lancet 353, 644.CrossRefGoogle ScholarPubMed
Levitan, C, Ward, PB, Catts, SV (1999). Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia. Biological Psychiatry 46, 955–962.Google Scholar
Lewis, DA, Levitt, P (2002). Schizophrenia as a disorder of neurodevelopment. Annual Review of Neuroscience 25, 409–432.CrossRefGoogle ScholarPubMed
McGuire, PK, David, AS, Murray, RM, Frackowiak, RSJ, Frith, CD, Wright, I, Silbersweig, DA (1995). Abnormal monitoring of inner speech: a physiological basis for auditory hallucinations. Lancet 346, 596–600.Google Scholar
Modinos, G, Costafreda, SG, van Tol, MJ, McGuire, PK, Aleman, A, Allen, P (2013). Neuroanatomy of auditory verbal hallucinations in schizophrenia: a quantitative meta-analysis of voxel-based morphometry studies. Cortex 49, 1046–1055.CrossRefGoogle ScholarPubMed
Moyer, CE, Shelton, MA, Sweet, RA (2015). Dendritic spine alterations in schizophrenia. Neuroscience Letters 601, 46–53.CrossRefGoogle ScholarPubMed
Mϕrch-Johnsen, L, Nesvåg, R, Jϕrgensen, KN, Lange, EH, Hartberg, CB, Haukvik, UK, Kompus, K, Westerhausen, R, Osnes, K, Andreassen, OA, Melle, I, Hugdahl, K, Agartz, I (2017). Auditory cortex characteristics in schizophrenia: associations with auditory hallucinations. Schizophrenia Bulletin 43, 75–83.Google Scholar
Neckelmann, G, Specht, K, Lund, A, Ersland, L, Smievoll, AI, Neckelmann, D, Hugdahl, K (2006). MR morphometry analysis of grey matter volume reduction in schizophrenia: association with hallucinations. International Journal of Neuroscience 116, 9–23.Google Scholar
Onitsuka, T, Shenton, ME, Salisbury, DF, Dickey, CC, Kasai, K, Toner, SK, Frumin, M, Kikinis, R, Jolesz, FA, McCarley, RW (2004). Middle and inferior temporal gyrus gray matter volume abnormalities in chronic schizophrenia: an MRI study. American Journal of Psychiatry 161, 1603–1611.CrossRefGoogle ScholarPubMed
Palaniyappan, L, Balain, V, Radua, J, Liddle, PF (2012). Structural correlates of auditory hallucinations in schizophrenia: a meta-analysis. Schizophrenia Research 137, 169–173.CrossRefGoogle ScholarPubMed
Panizzon, MS, Fennema-Notestine, C, Eyler, LT, Jernigan, TL, Prom-Wormley, E, Neale, M, Jacobson, K, Lyons, MJ, Grant, MD, Franz, CE, Xian, H, Tsuang, M, Fischl, B, Seidman, L, Dale, A, Kremen, WS (2009). Distinct genetic influences on cortical surface area and cortical thickness. Cerebral Cortex 19, 2728–2735.Google Scholar
Rajarethinam, RP, DeQuardo, JR, Nalepa, R, Tandon, R (2000). Superior temporal gyrus in schizophrenia: a volumetric magnetic resonance imaging study. Schizophrenia Research 41, 303–312.CrossRefGoogle ScholarPubMed
Rakic, P (1988). Specification of cerebral cortical areas. Science 241, 170–176.CrossRefGoogle ScholarPubMed
Rimol, LM, Hartberg, CB, Nesvåg, R, Fennema-Notestine, C, Hagler, DJ Jr., Pung, CJ, Jennings, RG, Haukvik, UK, Lange, E, Nakstad, PH, Melle, I, Andreassen, OA, Dale, AM, Agartz, I (2010). Cortical thickness and subcortical volumes in schizophrenia and bipolar disorder. Biological Psychiatry 68, 41–50.Google Scholar
Sanes, DH, Reh, TA, Harris, WA (2011). Development of the Nervous System. Academic Press: Burlington, MA.Google Scholar
Seal, ML, Aleman, A, McGuire, PK (2004). Compelling imagery, unanticipated speech and deceptive memory: neurocognitive models of auditory verbal hallucinations in schizophrenia. Cognitive Neuropsychiatry 9, 43–72.CrossRefGoogle ScholarPubMed
Selemon, LD, Goldman-Rakic, PS (1999). The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biological Psychiatry 45, 17–25.Google Scholar
Shergill, SS, Brammer, MJ, Williams, SCR, Murray, RM, McGuire, PK (2000). Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Archives of General Psychiatry 57, 1033–1038.Google Scholar
Sun, D, Stuart, GW, Jenkinson, M, Wood, SJ, McGorry, PD, Velakoulis, D, van Erp, TG, Thompson, PM, Toga, AW, Smith, DJ, Cannon, TD, Pantelis, C (2009). Brain surface contraction mapped in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Molecular Psychiatry 14, 976–986.Google Scholar
Tamnes, CK, Ostby, Y, Fjell, AM, Westlye, LT, Due-Tonnessen, P, Walhovd, KB (2010). Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cerebral Cortex 20, 534–548.Google Scholar
van Haren, NE, Schnack, HG, Cahn, W, van den Heuvel, MP, Lepage, C, Collins, L, Evans, AC, Hulshoff Pol, HE, Kahn, RS (2011). Changes in cortical thickness during the course of illness in schizophrenia. Archives of General Psychiatry 68, 871–880.CrossRefGoogle ScholarPubMed
van Swam, C, Federspiel, A, Hubl, D, Wiest, R, Boesch, C, Vermathen, P, Kreis, R, Strik, W, Dierks, T (2012). Possible dysregulation of cortical plasticity in auditory verbal hallucinations – a cortical thickness study in schizophrenia. Journal of Psychiatric Research 46, 1015–1023.CrossRefGoogle ScholarPubMed
Viechtbauer, W (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 1–48.CrossRefGoogle Scholar
Woodruff, P, Brammer, M, Mellers, J, Wright, I, Bullmore, E, Williams, S (1995). Auditory hallucinations and perception of external speech. Lancet 346, 1035.CrossRefGoogle ScholarPubMed
Xu, J, Wang, J, Fan, L, Li, H, Zhang, W, Hu, Q, Jiang, T (2015). Tractography-based parcellation of the human middle temporal gyrus. Scientific Reports 5, 18883.Google Scholar
Supplementary material: File

Cui supplementary material

Figure S1

Download Cui supplementary material(File)
File 175.4 KB