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

  • Y. Cui (a1) (a2) (a3), B. Liu (a1) (a2) (a3) (a4), M. Song (a1) (a2) (a3), D. M. Lipnicki (a5), J. Li (a1) (a2) (a3), S. Xie (a1) (a2) (a3), Y. Chen (a6), P. Li (a7) (a8), L. Lu (a7) (a8) (a9), L. Lv (a10) (a11), H. Wang (a6), H. Yan (a7) (a8), J. Yan (a7) (a8), H. Zhang (a10) (a11) (a12), D. Zhang (a7) (a8) (a9) and T. Jiang (a1) (a2) (a3) (a4) (a13) (a14)...



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.


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.


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.


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


Corresponding author

*Address for correspondence: Tianzi Jiang, Ph.D., Brainnetome Center, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, China. (Email:


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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, 175191.
Andreasen, NC, Flaum, M (1991). Schizophrenia: the characteristic symptoms. Schizophrenia Bulletin 17, 2749.
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, 14571462.
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, 192200.
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, 19982014.
Cabeza, R, Nyberg, L (2000). Imaging cognition II: an empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience 12, 147.
Catani, M, ffytche, DH (2005). The rises and falls of disconnection syndromes. Brain 128, 22242239.
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.
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179194.
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, 1105011055.
Fischl, B, Sereno, MI, Dale, AM (1999). Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195207.
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, 261276.
Frith, CD, Done, DJ (1988). Towards a neuropsychology of schizophrenia. British Journal of Psychiatry 153, 437443.
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.
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, 247255.
Glasser, MF, Rilling, JK (2008). DTI tractography of the human brain's language pathways. Cerebral Cortex 18, 24712482.
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, 81748179.
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, 467477.
Hoffman, RE (2008). Auditory/verbal hallucinations, speech perception neurocircuitry, and the social deafferentation hypothesis. Clinical EEG and Neuroscience 39, 8790.
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, 4956.
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, 7381.
Karnath, HO (2001). New insights into the functions of the superior temporal cortex. Nature Reviews Neuroscience 2, 568576.
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261276.
Lennox, BR, Park, SB, Jones, PB, Morris, PG (1999). Spatial and temporal mapping of neural activity associated with auditory hallucinations. Lancet 353, 644.
Levitan, C, Ward, PB, Catts, SV (1999). Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia. Biological Psychiatry 46, 955962.
Lewis, DA, Levitt, P (2002). Schizophrenia as a disorder of neurodevelopment. Annual Review of Neuroscience 25, 409432.
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, 596600.
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, 10461055.
Moyer, CE, Shelton, MA, Sweet, RA (2015). Dendritic spine alterations in schizophrenia. Neuroscience Letters 601, 4653.
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, 7583.
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, 923.
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, 16031611.
Palaniyappan, L, Balain, V, Radua, J, Liddle, PF (2012). Structural correlates of auditory hallucinations in schizophrenia: a meta-analysis. Schizophrenia Research 137, 169173.
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, 27282735.
Rajarethinam, RP, DeQuardo, JR, Nalepa, R, Tandon, R (2000). Superior temporal gyrus in schizophrenia: a volumetric magnetic resonance imaging study. Schizophrenia Research 41, 303312.
Rakic, P (1988). Specification of cerebral cortical areas. Science 241, 170176.
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, 4150.
Sanes, DH, Reh, TA, Harris, WA (2011). Development of the Nervous System. Academic Press: Burlington, MA.
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, 4372.
Selemon, LD, Goldman-Rakic, PS (1999). The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biological Psychiatry 45, 1725.
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, 10331038.
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, 976986.
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, 534548.
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, 871880.
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, 10151023.
Viechtbauer, W (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 148.
Woodruff, P, Brammer, M, Mellers, J, Wright, I, Bullmore, E, Williams, S (1995). Auditory hallucinations and perception of external speech. Lancet 346, 1035.
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.


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