Cited by 666Hallucinations in medical conditionsSchizophrenia research and treatmentMental Health and Psychiatry

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Mapping Auditory Hallucinations in Schizophrenia Using Functional Magnetic Resonance Imaging

Shergill, Sukhwinder S., Brammer, Michael J., Williams, Steven C. R., Murray, Robin M., McGuire, Philip K.·2000·Archives of General Psychiatry

DOI 10.1001/archpsyc.57.11.1033

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Abstract

BACKGROUND: Perceptions of speech in the absence of an auditory stimulus (auditory verbal hallucinations) are a cardinal feature of schizophrenia. Functional neuroimaging provides a powerful means of measuring neural activity during auditory hallucinations, but the results from previous studies have been inconsistent. This may reflect the acquisition of small numbers of images in each subject and the confounding effects of patients actively signaling when hallucinations occur. METHODS: We examined 6 patients with schizophrenia who were experiencing frequent auditory hallucinations, using a novel functional magnetic resonance imaging method that permitted the measurement of spontaneous neural activity without requiring subjects to signal when hallucinations occurred. Approximately 50 individual scans were acquired at unpredictable intervals in each subject while they were intermittently hallucinating. Immediately after each scan, subjects reported whether they had been hallucinating at that instant. Neural activity when patients were and were not experiencing hallucinations was compared in each subject and the group as a whole. RESULTS: Auditory hallucinations were associated with activation in the inferior frontal/insular, anterior cingulate, and temporal cortex bilaterally (with greater responses on the right), the right thalamus and inferior colliculus, and the left hippocampus and parahippocampal cortex (P<.0001). CONCLUSIONS: Auditory hallucinations may be mediated by a distributed network of cortical and subcortical areas. Previous neuroimaging studies of auditory hallucinations may have identified different components of this network.

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“Some functional studies also support the multiplicity of areas involved in AH (Shergill et al., 2000).”
Background
Functional connectivity of the temporo-parietal region in schizophrenia: Effects of rTMS treatment of auditory hallucinations
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“Some studies have reported involvement of right hemispheric language areas as well (Lennox et al., 2000; Shergill et al., 2000; Sommer et al., 2008).”
Background
Reduced neuronal activity in language-related regions after transcranial magnetic stimulation therapy for auditory verbal hallucinations
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“reported that the bilateral temporal lobes that work for speech processing are hyperactive during ongoing auditory hallucinations [179].”
Background
Effects of Psychotic State and Task Demand on Prefrontal Function in Schizophrenia: An fMRI Study of Overt Verbal Fluency
Fu, C. H. Y., John Suckling, A., Williams, S., Andrew, C., Vythelingum, G. N., & McGuire, P. K. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.3.485 · Cited by 112
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“Findings of morphometric changes also go together with altered neuronal activation during hallucinatory episodes, measured with fMRI or PET (Hubl et al., 2007; Shergill et al., 2000, Silbersweig et al., 1995; Woodruff et al., 1997).”
Background
Distinct processing of ambiguous speech in people with non-clinical auditory verbal hallucinations
Alderson-Day, B., Lima, C. F., Evans, S., Krishnan, S., Shanmugalingam, P., Fernyhough, C., & Scott, S. K. (2017) · Brain · doi:10.1093/brain/awx206 · Cited by 108
“ACC involvement was also observed in a number of early symptomcapture studies of people hearing voices while being scanned (Shergill et al., 2000), although later meta-analyses have failed to consistently identify this region during the hallucinatory state (Jardri et al., 2011; Kühn and Gallinat,…”
BackgroundResult
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Temporal course of auditory hallucinations
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“Recent neuroimaging studies suggest that both speech generation and perception areas are activated during auditory verbal hallucinations (Dierks et al, 1999; Lennox et al, 1999; Shergill et al, 2000), but the sequence in which these areas are activated remains unclear.”
Background
Mismatch Negativity Responses in Schizophrenia: A Combined fMRI and Whole-Head MEG Study
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“toms of the disease such as hallucinations (22, 23) and”
Background
Reality distortion is related to the structure of the salience network in schizophrenia
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“1998), but medial temporal overactivity has been reported in functional studies (Liddle et al. 1992 ; Silbersweig et al. 1995 ; Shergill et al. 2000).”
Background
Auditory hallucinations: Failure to inhibit irrelevant memories
Michie, P. T., Badcock, J. C., Waters, F. A. V., & Maybery, M. T. (2005) · Cognitive Neuropsychiatry · doi:10.1080/13546800344000363 · Cited by 104
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“…a reduced energy metabolism in the PFC which has been related with negative symptoms (Andreasen et al. 1997; Potkin et al. 2002) yet psychotic symptoms appear associated with hyperactivity of various cortical areas, including the PFC (Catafau et al. 1994; Dierks et al. 1999; Shergill et al. 2000).”
Background
An fMRI study of semantic processing in men with schizophrenia
Kubicki, M. R. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00383-5 · Cited by 106
“, 2001), studies investigating resting states in patients show increased activation in AC as well as STG, MTG, hippocampus, and the parahippocampal gyrus (Shergill et al., 2000; Silbersweig et al., 1995; Liddle et al., 1992).”
Background
Atypical hemispheric specialization for language in right-handed schizophrenia patients.
Dollfus, S., Razafimandimby, A., Delamillieure, P., Brazo, P., Joliot, M., Mazoyer, B., & Tzourio-mazoyer, N. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.009 · Cited by 99
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“The network involved in the generation of auditory hallucinations is probably more extended and has been well studied (McGuire et al, 1993; Shergill et al, 2000).”
BackgroundResult
The Application of DTI to Investigate White Matter Abnormalities in Schizophrenia
Kubicki, M. R., Westin, C., McCarley, R. W., & Shenton, M. E. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1340.024 · Cited by 99
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“…during hallucination versus non-hallucination periods, identifying wide-spread brain activation related to AVHs (Tiihonen et al., 1992; Silbersweig et al., 1995; Dierks et al., 1999; Lennox et al., 2000; Shergill et al., 2000; van de Ven et al., 2005; Hoffman et al., 2007; Sommer et al., 2008).”
Background
Processing of tactile information by the hippocampus
Pereira, A., Ribeiro, S. T. G., Wiest, M., Moore, L. C., Pantoja, J., Lin, S., & Nicolelis, M. A. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708611104 · Cited by 96
Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients
Plaze, M., David Bartrés-faz, A., Martinot, J., Januel, D., Bellivier, F., de Beaurepaire, R., Chanraud, S., Andoh, J., Lefaucheur, J., Eric Artiges, A., et al. (2006) · Schizophrenia Research · doi:10.1016/j.schres.2006.05.005 · Cited by 96
“, 1995), and medial or anterior temporal regions (Shergill et al., 2000; Silbersweig et al., 1995).”
Influential
Microstructural alterations of the arcuate fasciculus in schizophrenia patients with frequent auditory verbal hallucinations
de Weijer, A. D., Mandl, R. C. W., Diederen, K. M. J., Neggers, S. F. W., Kahn, R. S., Pol, H. E. H., & Sommer, I. E. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.05.010 · Cited by 101
“, 2010), such as the right and left temporo-parietal cortices and Broca's area and its right-sided homologue (Shergill et al., 2000; Sommer et al., 2003; Hoffman et al., 2007; Sommer et al., 2007; Sommer et al., 2008; Diederen et al., 2010).”
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Bentaleb, L. A., Beauregard, M., Liddle, P. F., & Stip, É. (2002) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0214 · Cited by 93
The role of the primary auditory cortex in the neural mechanism of auditory verbal hallucinations
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“This idea is supported by so-called “symptom capture” studies, which attempt to measure brain activity while subjects are experiencing AVHs (Woodruff et al., 1997; Dierks et al., 1999; Shergill et al., 2000).”
Background
Hearing voices: A role of interhemispheric auditory connectivity?
Mulert, C., Kirsch, V., Whitford, T. J., Alvarado, J., Pelavin, P. E., McCarley, R. W., Kubicki, M. R., Salisbury, D. F., & Shenton, M. E. (2011) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.570789 · Cited by 89
“…Magnetic Resonance Imaging (fMRI) and Positron Emission Tomography (PET) during AVH have both shown that activation of the auditory cortex is observed (Dierks et al. 1999; Shergill et al. 2000), as well as other regions including the inferior frontal cortex and the anterior cingulate cortex (ACC).”
Background
Psychotic Symptoms as a Continuum between Normality and Pathology
Stip, É., & Létourneau, G. (2009) · The Canadian Journal of Psychiatry · doi:10.1177/070674370905400302 · Cited by 90
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“The PANSS positive syndrome score is associated with the fusiform gyrus and middle temporal gyrus, which exhibit a regular pattern of reduction in complexity; previous studies have shown that these brain regions are associated with auditory or imaginary hallucinations [Lawrie et al., 2002; Santhouse et al., 2000; Sher…”
Result
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“…function and the production of hallucinations are overlapping (namely the superior temporal sulcus and inferior frontal gyrus; Kim et al., 2013), and the association between the latter (i.e., proneness to hallucinations) and unreliable sensory representations is commonplace (Shergill et al., 2000).”
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Takahashi, T., Wood, S. J., Soulsby, B., McGorry, P. D., Tanino, R., Suzuki, M., Velakoulis, D., & Pantelis, C. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2008.12.029 · Cited by 90
“Gray matter reduction or dysfunction of the insula has been implicated in manifesting psychotic symptoms (Crespo-Facorro et al., 2000; Shapleske et al., 2002; Shergill et al., 2000) and cognitive impairments (Crespo-Facorro et al., 2001a,b; Curtis et al., 1998).”
Influential
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Simons, C. J. P., Tracy, D. K., Sanghera, K. K., O'Daly, O., Gilleen, J., Dominguez, M.-D.-G., Krabbendam, L., & Shergill, S. S. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.007 · Cited by 87
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Male and female voices activate distinct regions in the male brain
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A neural basis for the perception of voices in external auditory space
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“We have used fMRI and a virtual acoustics paradigm to implicate left PT in the perception of voices in external auditory space.”
BackgroundMethodInfluential
Auditory hallucinations: A review of the ERC “VOICE” project
Hugdahl, K. (2015) · World Journal of Psychiatry · doi:10.5498/wjp.v5.i2.193 · Cited by 93
Neuroanatomy and neurophysiology in schizophrenia
Kasai, K., Iwanami, A., Yamasue, H., Kuroki, N., Nakagome, K., & Fukuda, M. (2002) · Neuroscience Research · doi:10.1016/s0168-0102(02)00023-8 · Cited by 87
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Saba, G., Verdon, C.-M., Kalalou, K., Rocamora, J.-F., Dumortier, G., Benadhira, R., Stamatiadis, L., Vicaut, É., Lipski, H., & Januel, D. (2005) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2005.02.008 · Cited by 87
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“…auras (Hogan and Kaiboriboon, 2004), hearing a favorite and familiar song (Fischer et al., 2004; Ozsarac et al., in press), the perception of ‘‘voices” in paranoid schizophrenics (Dierks et al., 1999; Shergill et al., 2000) and musical hallucinations in Alzheimer’s disease (Mori et al., 2006).”
Background
Morphologic alterations of the parcellated superior temporal gyrus in schizophrenia spectrum
Takahashi, T., Suzuki, M., Zhou, S.-Y., Tanino, R., Hagino, H., Kawasaki, Y., Matsui, M., Seto, H., & Kurachi, M. (2006) · Schizophrenia Research · doi:10.1016/j.schres.2006.01.016 · Cited by 86
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Transcranial magnetic stimulation (TMS) for schizophrenia
Dougall, N. J., Maayan, N., Soares‐Weiser, K., McDermott, L. M., & McIntosh, A. M. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd006081.pub2 · Cited by 86
Clozapine but not Haloperidol Re-establishes Normal Task-Activated rCBF Patterns in Schizophrenia within the Anterior Cingulate Cortex
Lahti, A. C., Holcomb, H. H., Weiler, M. A., Medoff, D. R., Frey, K., Hardin, M. G., & Tamminga, C. A. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300312 · Cited by 84
“…that the ACC is involved in a distributed neural network that mediates psychosis (Cleghorn et al, 1992; Silbersweig et al, 1995; Szechtman et al, 1998; Shergill et al, 2000). rCBF in ACC significantly correlates with psychosis levels in unmedicated SV (Tamminga et al, 2001; Lee et al, 2003).”
Background
Should We Treat Auditory Hallucinations with Repetitive Transcranial Magnetic Stimulation? A Metaanalysis
Tranulis, C., Sepehry, A. A., Galinowski, A., & Stip, É. (2008) · The Canadian Journal of Psychiatry · doi:10.1177/070674370805300904 · Cited by 84
The hearing hippocampus
Billig, A. J., Lad, M., Sedley, W., & Griffiths, T. D. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102326 · Cited by 92
“Within-subjects comparisons have revealed greater (para)hippocampal activity for periods with auditory hallucinations compared to those without (Dierks et al., 1999; Raij et al., 2009; Shergill, 2001; Shergill et al., 2000; Silbersweig et al., 1995).”
Background
Neural correlates of syntax production in schizophrenia
Kircher, T. T. J., Oh, T. M., Brammer, M. J., & McGuire, P. K. (2005) · The British Journal of Psychiatry · doi:10.1192/bjp.186.3.209 · Cited by 84
Transcranial magnetic stimulation of Wernicke's and right homologous sites to curtail “voices”: a randomized trial
Hoffman, R. E., Wu, K., Pittman, B., Cahill, J. D., Hawkins, K. A., Fernandez, T., & Hannestad, J. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.01.016 · Cited by 82
Auditory hallucinations: Insights and questions from neuroimaging
Woodruff, P. W. R. (2004) · Cognitive Neuropsychiatry · doi:10.1080/13546800344000165 · Cited by 82
Brain structural changes in schizophrenia patients with persistent hallucinations
O’Daly, O., Frangou, S., Chitnis, X. A., & Shergill, S. S. (2007) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2007.03.001 · Cited by 86
“Their functional substrates have recently been found to include frontal and temporal cortical regions (Dierks et al., 1999; Shergill et al., 2000), in accord with contemporary cognitive models emphasising fronto-temporal disconnectivity (Frith et al., 2000).”
BackgroundResult
Resting-state fMRI mapping of cerebellar functional dysconnections involving multiple large-scale networks in patients with schizophrenia
Chen, Y., Tu, P., Lee, Y.-C., Chen, Y.-S., Li, C., & Su, T. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.05.029 · Cited by 80
Anatomical Evidence of Impaired Feedforward Auditory Processing in Schizophrenia
Sweet, R. A., Bergen, S. E., Sun, Z., Marcsisin, M. J., Sampson, A. R., & Lewis, D. A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.07.033 · Cited by 81
Aberrations in the arcuate fasciculus are associated with auditory verbal hallucinations in psychotic and in non‐psychotic individuals
de Weijer, A. D., Neggers, S. F. W., Diederen, K. M. J., Mandl, R. C. W., Kahn, R. S., Pol, H. E. H., & Sommer, I. E. (2011) · Human Brain Mapping · doi:10.1002/hbm.21463 · Cited by 86
“Its exact pathophysiology remains elusive, although functional MRI studies suggest the involvement of the language system [Diederen et al., 2010; Ford et al., 2007; Heinks-Maldonado et al., 2007; Jardri et al., 2010; Shergill et al., 2000; Sommer et al., 2008; Whitford et al., 2010].”
Background
Source-based morphometry of gray matter volume in patients with schizophrenia who have persistent auditory verbal hallucinations.
Kubera, K., Sambataro, F., Vasić, N., Wolf, N. D., Frasch, K., Hirjak, D., Thomann, P. A., & Wolf, R. C. (2014) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.11.015 · Cited by 83
Aberrant connectivity during self–other source monitoring in schizophrenia
Wang, L. Y., Metzak, P. D., & Woodward, T. S. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.11.012 · Cited by 85
“…notation that aspects of the illness considered a disorder of “self” (e.g., hallucinations and Schneiderian delusions) may be associated with activation in the same parts of frontal and temporal cortices that are normally engaged during perception of external information (Shergill et al., 2000a).”
Background
Psychosis and autism: magnetic resonance imaging study of brain anatomy
Toal, F., Bloemen, O., Deeley, Q., Tunstall, N., Daly, E., Page, L., Brammer, M. J., Murphy, K. C., & Murphy, D. (2009) · The British Journal of Psychiatry · doi:10.1192/bjp.bp.107.049007 · Cited by 83
A 20-year multi-follow-up of hallucinations in schizophrenia, other psychotic, and mood disorders
Goghari, V. M., Harrow, M., Grossman, L. S., & Rosen, C. (2012) · Psychological Medicine · doi:10.1017/s0033291712002206 · Cited by 78
“Last, there is an increasing literature documenting biological mechanisms that may be involved in hallucinations (Shergill et al. 2000 ; Hubl et al. 2004 ; Goghari et al. 2010 ; Jardri et al. 2011) ; however, this literature needs to be supplemented with research on the phenomenology and theoretical significance of ha…”
Background
Use of Repetitive Transcranial Magnetic Stimulation for Treatment in Psychiatry
Aleman, A. (2013) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2013.11.2.53 · Cited by 84
Impairment of inhibitory control processing related to acute psychotomimetic effects of cannabis
Bhattacharyya, S., Atakan, Z., Martín‐Santos, R., Crippa, J. A. S., Kambeitz, J. P., Malhi, S., Giampietro, V., Williams, S., Brammer, M. J., Rubia, K., et al. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.11.018 · Cited by 81
“Altered inferior frontal activation has previously been implicated in the pathophysiology of psychotic symptoms in schizophrenia (Shergill et al., 2000).”
Background
Structural covariance in the hallucinating brain: a voxel-based morphometry study
Modinos, G., Vercammen, A., Mechelli, A., Knegtering, H., McGuire, P. K., & Aleman, A. (2009) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0958 · Cited by 78
Patterns of anterior cingulate activation in schizophrenia: a selective review
Adams, R. A., & David, A. S. (2007) · Neuropsychiatric Disease and Treatment · doi:10.2147/nedt.2007.3.1.87 · Cited by 83
“Numerous imaging studies have shown the ACC to be hyperactive in schizophrenics during auditory verbal hallucinations (Silbersweig et al 1995; Shergill et al 2000; Copolov et al 2003) and passivity phenomena (Spence et al 1997), although whether this refl ects an attentional or a generative process…”
Background
Regional dopamine synthesis in patients with schizophrenia using L-[β-11C]DOPA PET
Nozaki, S., Kato, M., Takano, H., Ito, H., Takahashi, H., Arakawa, R., Okumura, M., Fujimura, Y., Matsumoto, R., Ota, M., et al. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2008.11.006 · Cited by 74
“Previous functional MRI studies have demonstrated the involvement of the right temporal cortex in some of the positive symptoms such as auditory hallucination (Shergill et al., 2000;Woodruff et al., 1997) and formal thought disorder (Kircher et al., 2002) in schizophrenia.”
Auditory change detection in schizophrenia: sources of activity, related neuropsychological function and symptoms in patients with a first episode in adolescence, and patients 14 years after an adolescent illness-onset
Oades, R. D., Wild–Wall, N., Juran, S. A., Sachsse, J., Oknina, L. B., & Röpcke, B. (2006) · BMC Psychiatry · doi:10.1186/1471-244x-6-7 · Cited by 76
“This is consistent with the attribution of these symptoms to impaired functional connectivity between the temporal and frontal lobes [79,80].”
Background
Testing models of thalamic dysfunction in schizophrenia using neuroimaging
Sim, K., Cullen, T. J., Öngür, D., & Heckers, S. (2005) · Journal of Neural Transmission · doi:10.1007/s00702-005-0363-8 · Cited by 75
“Abnormalities of the thalamus which were found in uncontrolled studies of patients experiencing auditory hallucinations (Shergill et al., 2000a; Silbersweig et al., 1995) were corroborated by more recent findings from a controlled study (Shergill et al., 2000b) which found auditory verbal imagery…”
Contribution of hippocampal region CA3 to consciousness and schizophrenic hallucinations
Behrendt, R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.12.009 · Cited by 75
“The actual experience of auditory verbal hallucinations (Shergill et al., 2000) or visual hallucinations is accompanied by hippocampal activation in fMRI, along with activations in higher-order neocortical sensory-processing areas (Oertel et al., 2007).”
A pilot double-blind sham-controlled trial of repetitive transcranial magnetic stimulation for patients with refractory schizophrenia treated with clozapine
de Jesus, D. R., Gil, A., Barbosa, L., Lobato, M. I. R., Magalhães, P. V. D. S., Favalli, G. P. D. S., Marcolin, M. A., Daskalakis, Z. J., & Belmonte-de-Abreu, P. S. (2010) · Psychiatry Research · doi:10.1016/j.psychres.2010.11.022 · Cited by 75
“Neuroimaging studies suggest that activation of brain regions underlying speech perception play a role in producing AHs (Dierks et al., 1999; Shergill et al., 2000; Suzuki et al., 1993; Silbersweig et al., 1995; Lennox et al., 2000; Woodruff et al., 1994, 1997).”
Background
Hyperactivity, decreased startle reactivity, and disrupted prepulse inhibition following disinhibition of the rat ventral hippocampus by the GABAA receptor antagonist picrotoxin
Bast, T., Zhang, W.-N., & Feldon, J. (2001) · Psychopharmacology · doi:10.1007/s002130100775 · Cited by 73
The cortical microstructural basis of lateralized cognition: a review
Chance, S. A. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00820 · Cited by 74
“The auditory region offers one www.frontiersin.org July 2014 | Volume 5 | Article 820 | 5 of the clearest associations between psychotic symptoms and brain structure, as it is activated during auditory hallucinations (Shergill et al., 2000; Ropohl et al., 2004).”
Background
Functional Brain Imaging in Schizophrenia: Selected Results and Methods
Brown, G. G., & Thompson, W. K. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_54 · Cited by 75
Functional MRI of Verbal Self-monitoring in Schizophrenia: Performance and Illness-Specific Effects
Kumari, V., Fannon, D. G., Ffytche, D. H., Raveendran, V., Antonova, E., Premkumar, P., Cooke, M. A., Anilkumar, A. P., Williams, S., Andrew, C., et al. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn148 · Cited by 76
“Previous studies examining auditory verbal imagery have observed normal frontal but reduced TL activity in patients with schizophrenia when they were required to imagine words spoken by others.(14,15,45,46) The auditory verbal imagery paradigms, however, may not exert the same, timeconstrained, load on the verbal WM s…”
Background
Auditory verbal hallucinations are related to cortical thinning in the left middle temporal gyrus of patients with schizophrenia
Cui, Y. J., Liu, B., Song, M., Lipnicki, D. M., Li, J., Xie, S., Chen, Y., Li, P., Lü, L., Lv, L., et al. (2017) · Psychological Medicine · doi:10.1017/s0033291717001520 · Cited by 74
“Functional studies have implicated the left MTG in this process, with the area showing reduced activation in schizophrenia patients with AVHs during a task that involved monitoring inner speech (McGuire et al. 1995; Shergill et al. 2000).”
Proteomic analysis reveals protein changes within layer 2 of the insular cortex in schizophrenia
Pennington, K., Dicker, P., Dunn, M. J., & Cotter, D. (2008) · PROTEOMICS · doi:10.1002/pmic.200800415 · Cited by 72
“The insular cortex (IC) is a brain region that has been shown to be involved in auditory hallucinations and language [1].”
Background
The Perceptual Characteristics of Voice-Hallucinations in Deaf People: Insights into the Nature of Subvocal Thought and Sensory Feedback Loops
Atkinson, J. R. (2005) · Schizophrenia Bulletin · doi:10.1093/schbul/sbj063 · Cited by 74
“ing voice-hallucinations show activity in the auditory association cortex, rather than primary auditory areas.(27)”
Brain-imaging studies of language production
Indefrey, P. (2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780198568971.013.0033 · Cited by 72
Short and Long Term Effects of Left and Bilateral Repetitive Transcranial Magnetic Stimulation in Schizophrenia Patients with Auditory Verbal Hallucinations: A Randomized Controlled Trial
Bais, L., Vercammen, A., Stewart, R. E., van Es, F., Visser, B., Aleman, A., & Knegtering, H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108828 · Cited by 69
“AVH have been related to both structural and functional anomalies in frontal, temporal and parietal regions [3,4].”
Increased water diffusivity in the frontal and temporal cortices of schizophrenic patients
Shin, Y., Kwon, J. S., Ha, T. H., Park, H., Kim, D. J., Hong, S., Moon, W., Lee, J. M., Kim, I. Y., Kim, S. I., et al. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.11.017 · Cited by 68
“All of these regions constitute primary brain loci which manifest structural, functional and sometimes histological abnormalities in schizophrenics (Akbarian et al., 1996; Shergill et al., 2000; Shenton et al., 2001; Kirkpatrick et al., 2003).”
Background
Interhemispheric auditory connectivity: structure and function related to auditory verbal hallucinations
Steinmann, S., Leicht, G., & Mulert, C. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00055 · Cited by 68
Cortical activity associated with auditory hallucinations
Ropohl, A., Sperling, W., Elstner, S., Tomandl, B., Reulbach, U., Kaltenhäuser, M., Kornhuber, J., & Maihöfner, C. (2004) · NeuroReport · doi:10.1097/00001756-200403010-00028 · Cited by 67
Grey matter deficits and symptom profile in first episode schizophrenia
Whitford, T. J., Farrow, T. F. D., Gomes, L. J., Brennan, J., Harris, A. W. F., & Williams, L. M. (2005) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2005.05.010 · Cited by 67
“Furthermore, abnormal activations in the inferior parietal cortex have been found to be associated with hallucinations (Shergill et al., 2000) and passivity delusions (Spence et al.”
Background
Targeting the Hippocampal Mossy Fiber Synapse for the Treatment of Psychiatric Disorders
Kobayashi, K. (2009) · Molecular Neurobiology · doi:10.1007/s12035-008-8049-5 · Cited by 70
“Magnetic resonance imaging (MRI) studies have consistently demonstrated a reduction in the hippocampus volume in patients with psychiatric disorders [1–3] and functional MRI studies have shown changes in the hippocampal activity that are associated with symptoms of psychiatric disorders [4, 5].”
Background
Aberrant connectivity of areas for decoding degraded speech in patients with auditory verbal hallucinations
Clos, M., Diederen, K. M. J., Meijering, A. L., Sommer, I. E., & Eickhoff, S. B. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0519-5 · Cited by 70
“Previously, observations of reduced SMA response in AVH compared with deliberate imagining alien speech (Shergill et al. 2000) and in verbal imagery in schizophrenic patients with AVH compared with healthy controls and schizophrenic patients without AVH (McGuire et al.”
Background
Chronic schizophrenia as a brain misconnection syndrome: a white matter voxel-based morphometry study
Spalletta, G., Tomaiuolo, F., Marino, V., Bonaviri, G., Trequattrini, A., & Caltagirone, C. (2003) · Schizophrenia Research · doi:10.1016/s0920-9964(03)00010-0 · Cited by 67
“Interestingly, the results of our study are in line with those in which structural and functional changes (Barta et al., 1990; Cleghorn et al., 1992; Gomez, 2002; Holinger et al., 1999; Lawrie et al., 2002; Levitan et al., 1999; Shergill et al., 2000) and electroencephalographic abnormalities (Ford et al.”
Result
The cognitive and anatomo-functional basis of reality distortion in schizophrenia: A view from memory event-related potentials
Guillem, F., Bicu, M., Pampoulova, T., Hooper, R., Bloom, D., Wolf, M.-A., Messier, J., Desautels, R., Todorov, C., Lalonde, P., et al. (2003) · Psychiatry Research · doi:10.1016/s0165-1781(03)00003-9 · Cited by 66
“1996) or delusion and hallucination as single entities (Sabri et al., 1997; Shergill et al., 2000).”
Background
Structural Analysis of Heschl’s Gyrus in Schizophrenia Patients with Auditory Hallucinations
Hubl, D., Dougoud-Chauvin, V., Zeller, M., Federspiel, A., Boesch, C., Strik, W. K., Dierks, T., & Koenig, T. W. (2009) · Neuropsychobiology · doi:10.1159/000258637 · Cited by 69
A sham-controlled trial of left and right temporal rTMS for the treatment of auditory hallucinations
Loo, C. K. A., Sainsbury, K., Mitchell, P. B., Hadži-Pavlović, D., & Sachdev, P. S. (2009) · Psychological Medicine · doi:10.1017/s0033291709990900 · Cited by 64
“Most studies to date have trialled rTMS to the left temporoparietal area ; however, both right and left temporal activation have been associated with auditory hallucinations in neuroimaging studies (Shergill et al. 2000 ; Sommer et al. 2007).”
Background
Altered Glutamate Protein Co-Expression Network Topology Linked to Spine Loss in the Auditory Cortex of Schizophrenia
MacDonald, M. L., Ding, Y., Newman, J. T., Hemby, S. E., Penzes, P., Lewis, D. A., Yates, N. A., & Sweet, R. A. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.09.006 · Cited by 65
Structural Alterations of the Social Brain: A Comparison between Schizophrenia and Autism
Radeloff, D., Ciaramidaro, A., Siniatchkin, M., Hainz, D., Schlitt, S., Weber, B., Poustka, F., Bölte, S., Walter, H., & Freitag, C. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106539 · Cited by 67
“Functional and structural studies revealed that the insula, along with regions traditionally known as language areas, seem to play a key role in auditory hallucinations in SCZ [86–92]: A Insula dysfunction might cause a confusion of the two sources, resulting in internal sensory information being attributed to externa…”
Background
Neuronal correlates of visual and auditory alertness in the DMT and ketamine model of psychosis
Daumann, J., Wagner, D. R., Heekeren, K., Neukirch, A., Thiel, C. M., & Gouzoulis‐Mayfrank, E. (2009) · Journal of Psychopharmacology · doi:10.1177/0269881109103227 · Cited by 62
An fMRI Study of Functional Abnormalities in the Verbal Working Memory System and the Relationship to Clinical Symptoms in Chronic Schizophrenia
Hashimoto, R., Lee, K., Preus, A. P., McCarley, R. W., & Wible, C. G. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp079 · Cited by 62
Left hemisphere lateralisation of auditory hallucinations in schizophrenia: A dichotic listening study
Hugdahl, K., L⊘berg, E.-M., J⊘rgensen, H. A., Lundervold, A., Lund, A., Green, M. F., & Rund, B. R. (2008) · Cognitive Neuropsychiatry · doi:10.1080/13546800801906808 · Cited by 61
Repetitive transcranial magnetic stimulation and transcranial direct current stimulation for auditory hallucinations in schizophrenia: Systematic review and meta-analysis
Guttesen, L. L., Albert, N., Nordentoft, M., & Hjorthøj, C. R. (2021) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2021.09.001 · Cited by 59
Medial Frontal Hyperactivity in Reality Distortion
Taylor, S. F., Welsh, R. C., Chen, A. C., Velander, A. J., & Liberzon, I. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.11.029 · Cited by 58
Neural functional organization of hallucinations in schizophrenia: multisensory dissolution of pathological emergence in consciousness.
Jardri, R., Pins, D., Bubrovszky, M., Lucas, B., Lethuc, V., Delmaire, C., Vantyghem, V., Despretz, P., & Thomas, P. (2009) · Consciousness and Cognition · doi:10.1016/j.concog.2008.12.009 · Cited by 57
“Moreover, the ACC has already been shown to be activated during hallucinatory episodes (Lennox et al., 1999; Shergill et al., 2000; Silbersweig et al., 1995), and some authors have proposed that hyperactivation of the ACC may reflect the incapacity for these patients to correct for ambiguous…”
Background
Comparison of structural covariance with functional connectivity approaches exemplified by an investigation of the left anterior insula
Clos, M., Rottschy, C., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.05.030 · Cited by 63
“…insular involvement in schizophrenic symptoms including auditory–verbal hallucinations (Clos et al., 2014; Dierks et al., 1999; Hoffman et al., 2008; Shergill et al., 2000; Sommer et al., 2008), impairment of verbal fluency (Curtis et al., 1998), working memory (Glahn et al., 2005; Hashimoto et…”
Background
fMRI Activity Correlated With Auditory Hallucinations During Performance of a Working Memory Task: Data From the FBIRN Consortium Study
Wible, C. G., Lee, K.-E., Molina, I., Hashimoto, R., Preus, A. P., Roach, B. J., Ford, J. M., Mathalon, D. H., McCarthey, G., Turner, J. A., et al. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn142 · Cited by 59
Transcranial Magnetic Stimulation for Schizophrenia
Dougall, N. J., Maayan, N., Soares‐Weiser, K., McDermott, L., & McIntosh, A. M. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv121 · Cited by 55

Authors: Shergill, S. S., Brammer, M. J., Williams, S. C. R., Murray, R. M., & McGuire, P. K.
Affiliations: King's College London (GB)
ORCID: Shergill, Sukhwinder S.
Brammer, Michael J.
Williams, Steven C. R.
Murray, Robin M.
McGuire, Philip K.
Venue: Archives of General Psychiatry
Publisher: American Medical Association (AMA)
Published: 2000-11-01
Volume: 57
Issue: 11
Pages: 1033
ISSN: 0003-990X (ISSN-L)
DOI: 10.1001/archpsyc.57.11.1033
OpenAlex: W2022503841
Cited by: 666
References: 36
Citations by year: 2026: 11 · 2025: 13 · 2024: 12 · 2023: 18 · 2022: 20 · 2021: 14 · 2020: 13 · 2019: 17 · 2018: 22 · 2017: 20 · 2016: 22 · 2015: 20 · 2014: 28 · 2013: 30 · 2012: 43
FWCI: 11.08
Type: journal article
Language: en
Open access: closed
Locations: Archives of General Psychiatry (publishedVersion)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Hallucinations in medical conditions
Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Social Sciences › Arts and Humanities › Philosophy › Mental Health and Psychiatry
Keywords: auditory verbal hallucinations, schizophrenia, spontaneous neuronal activity, inferior frontal cortex, insula, anterior cingulate cortex, thalamus, inferior colliculus, hippocampus, parahippocampal cortex, temporal cortex, distributed neural networks
MeSH terms: Auditory Perception, Brain Mapping, Hallucinations, Humans, Magnetic Resonance Imaging, Schizophrenia, Schizophrenic Psychology

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Mapping Auditory Hallucinations in Schizophrenia Using Functional Magnetic Resonance Imaging

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