Cited by 651Hallucinations in medical conditionsSchizophrenia research and treatmentMental Health and Psychiatry

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Cortical Activations During Auditory Verbal Hallucinations in Schizophrenia: A Coordinate-Based Meta-Analysis

Jardri, Renaud, Pouchet, Alexandre, Pins, Delphine, Thomas, Pierre·2011·American Journal of Psychiatry

DOI 10.1176/appi.ajp.2010.09101522

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Abstract

OBJECTIVE: Auditory verbal hallucinations (AVHs) constitute severe, incapacitating symptoms of schizophrenia. Despite increasing interest in the functional exploration of AVHs, the available findings remain difficult to integrate because of their considerable variability. The authors' aim was to perform a robust quantitative review of existing functional data in order to elucidate consistent patterns observed during the emergence of AVHs and to orient new pathophysiological models of hallucinations. METHOD: Ten positron emission tomography or functional magnetic resonance imaging studies were selected for the meta-analysis after systematic review. A total of 68 patients with schizophrenia spectrum disorders experiencing AVHs during scanning were included. According to a random-effects activation likelihood estimation algorithm, stereotaxic coordinates of 129 foci, reported as significant in the source studies, were extracted and computed to estimate the brain locations most consistently associated with AVHs across studies (cluster-extent threshold: 200 mm³). RESULTS: Patients experiencing AVHs demonstrated significantly increased activation likelihoods in a bilateral neural network, including the Broca's area (activation likelihood estimation=1.84×10⁻³), anterior insula (1.78×10⁻³), precentral gyrus (1.46×10⁻³), frontal operculum (1.29×10⁻³), middle and superior temporal gyri (1.59×10⁻³), inferior parietal lobule (1.33×10⁻³), and hippocampus/parahippocampal region (1.90×10⁻³). CONCLUSIONS: This meta-analysis demonstrated that experiencing AVHs is associated with increased activity in fronto-temporal areas involved in speech generation and speech perception, but also within the medial temporal lobe, a structure notably involved in verbal memory. Such findings support a model for AVHs in which aberrant cortical activations emerge within a distributed network involved at different levels of complexity in the brain architecture. Critical future directions are considered.

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“For example, a meta-analysis of AVH fMRI studies showed that AVH was associated with increased activities in speech generation areas such as the inferior frontal gyrus and insula [7].”
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“For example, researchers working with patients with schizophrenia have used this approach to identify the neural activation patterns associated with verbal hallucinations by asking patients suffering from auditory verbal hallucinations to report the on- and offset of the voices [20-22].”
Background
Empathy in schizophrenia: neural alterations during emotion recognition and affective sharing
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“The IFG is also part of a robust network active in auditory verbal hallucinations that are often present in patients with SCZ (69).”
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Quantifying auditory impressions in dreams in order to assess the relevance of dreaming as a model for psychosis
Fosse, R., & Larøi, F. (2020) · PLoS ONE · doi:10.1371/journal.pone.0230212 · Cited by 11
Targeted effects of ketamine on perceptual expectation during mediated learning in rats
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“2017) and auditory-verbal hallucinations generally (Jardri et al. 2011).”
The phenomenology of auditory verbal hallucinations in schizophrenia and the challenge from pseudohallucinations
López‐Silva, P., Álvaro Cavieres, F., & Humpston, C. S. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.826654 · Cited by 15
Short Association Fibres of the Insula-Temporoparietal Junction in Early Psychosis: A Diffusion Tensor Imaging Study
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Different and Shared Brain Volume Abnormalities in Late- and Early-Onset Schizophrenia
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Circular inference predicts nonuniform overactivation and dysconnectivity in brain-wide connectomes
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Self-citation
Relationship Between White Matter Microstructure and Hallucination Severity in the Early Stages of Psychosis: A Diffusion Tensor Imaging Study
Sato, Y., Sakuma, A., Ohmuro, N., Katsura, M., Abe, K., Tomimoto, K., Iizuka, K., Ito, F., Tomita, H., & Matsumoto, K. (2021) · Schizophrenia Bulletin Open · doi:10.1093/schizbullopen/sgab015 · Cited by 9
Impact of Repetitive Transcranial Magnetic Stimulation (rTMS) on Brain Functional Marker of Auditory Hallucinations in Schizophrenia Patients
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“Some authors endeavored to capture the neural signature of the AVH by asking patients to signal the occurrence of AVH while they were being scanned (for meta-analysis see [2–7]).”
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Hallucinations de l’enfant et de l’adolescent
Jardri, R., Bonelli, F., Askénazy, F., Georgieff, N., & Delion, P. (2013) · International Conference on Embedded and Multimedia Computing · doi:10.1016/s0246-1072(13)58150-8 · Cited by 10
Self-citation
Paracingulate Sulcus Length and Cortical Thickness in Schizophrenia Patients With and Without a Lifetime History of Auditory Hallucinations
Ćurĉić‐Blake, B., de Vries, A., Renken, R. J., Marsman, J.-B., Garrison, J. R., Hugdahl, K., & Aleman, A. (2023) · Schizophrenia Bulletin · doi:10.1093/schbul/sbac072 · Cited by 11
“5 As a key region, involvement of the superior temporal lobe, including the temporoparietal junction (speech perception area) has been consistently found, which may correspond to the perceptual aspect.”
Background
Progressive loss of cortical gray matter in first episode psychosis patients with auditory hallucinations
García‐Martí, G., Escartí, M. J., Nácher, J., Pérez-Rando, M., Mané, A., Usall, J., Berrocoso, E., Pomarol‐Clotet, E., López-Ilundain, J. M., Cuesta, M. J., et al. (2023) · Schizophrenia Research · doi:10.1016/j.schres.2023.11.011 · Cited by 10
The efficacy and safety of continuous theta burst stimulation for auditory hallucinations: a systematic review and meta-analysis of randomized controlled trials
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“The temporo-parietal junction (TPJ) is a connection of the primary (PAC) and secondary (SAC) auditory cortices and showed overactivity during episodes of auditory verbal hallucinations (23).”
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What Can Neuroscience Tell Us about the Hard Problem of Consciousness?
Brogaard, B. “., & Gatzia, D. E. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00395 · Cited by 11
“Reduction in the prefrontal functional connectivity was found in studies using functional magnetic resonance imaging (fMRI) on eight schizophrenia patients and 10 controls in schizophrenia suffering from auditory hallucinations (Lawrie et al., 2002; see also Jardri et al., 2011; Allen et al., 2012).”
BackgroundInfluential
Neuroscience for Clinicians: Translational Clinical Neuroscience to Inspire Clinical Practice and Research
Li, H., Goldin, P. R., & Siegle, G. J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-818697-8.00190-4 · Cited by 11
AUDITORY HALLUCINATIONS ELICIT SIMILAR BRAIN ACTIVATION IN PSYCHOTIC AND NON-PSYCHOTIC INDIVIDUALS
Sommer, I. E. (2012) · Schizophrenia Research · doi:10.1016/s0920-9964(12)70250-5 · Cited by 10
Local versus long-range connectivity patterns of auditory disturbance in schizophrenia
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“, 2017), anterior insula (Jardri et al., 2011; Powers et al., 2017), striatum (Cassidy et al.”
BackgroundResultInfluential
Alterations in brain connectivity patterns in schizophrenia patients with auditory verbal hallucinations during low frequency repetitive transcranial magnetic stimulation
Xie, Y., Guan, M., Wang, Z., Ma, Z., Wang, H., & Fang, P. (2023) · Psychiatry Research · doi:10.1016/j.psychres.2023.115457 · Cited by 10
“A meta-analysis showed heightened activation in this area in schizophrenia patients experiencing AVH (Jardri et al., 2011).”
An investigation of the neural association between auditory imagery and perception of complex sounds
Gu, J., Zhang, H., Liu, B., Li, X., Wang, P., & Wang, B. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01948-z · Cited by 11
The Neurochemistry of Schizophrenia
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Candidate Genes Involved in the Expression of Psychotic Symptoms: A Focus on Hallucinations
Sanjuán, J., Moltó, M. D., & Tolosa, A. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4121-2_13 · Cited by 10
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Auditory Verbal Hallucinations in Psychosis
Mitropoulos, G. B. (2019) · The Journal of Nervous and Mental Disease · doi:10.1097/nmd.0000000000001089 · Cited by 9
“The sensoryperceptive quality of the symptoms might also be seen in the light of the hypothesis of aberrant activations within sensorimotor cortices, which is supported by the findings of Jardri et al. (2011).”
BackgroundResult
Structural Neuroimaging in Psychotic Patients with Auditory Verbal Hallucinations
Allen, P., & Modinos, G. (2011) · Springer eBooks · doi:10.1007/978-1-4614-0959-5_19 · Cited by 9
Association Between Connectivity of Hippocampal Sub-Regions and Auditory Verbal Hallucinations in Schizophrenia
Liu, L., Cui, L., Xi, Y., Wang, X., Liu, Y., Xu, Z., Wang, H., Yin, H. J., & Qin, W. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00424 · Cited by 9
Explications cognitives des hallucinations acoustico-verbales dans la schizophrénie : un article de synthèse de la littérature scientifique
Livet, A., & Salomé, F. (2020) · L Encéphale · doi:10.1016/j.encep.2019.11.010 · Cited by 9
Impaired self-recognition in individuals with no full-blown psychotic symptoms represented across the continuum of psychosis: a meta-analysis
Lavallé, L., Dondé, C., Gawęda, Ł., Brunelin, J., & Mondino, M. (2020) · Psychological Medicine · doi:10.1017/s003329172000152x · Cited by 12
The Visual Word Form Area compensates for auditory working memory dysfunction in schizophrenia
Herman, A. B., Brown, E. G., Dale, C. L., Hinkley, L. B. N., Subramaniam, K., Houde, J. F., Fisher, M., Vinogradov, S., & Nagarajan, S. S. (2020) · Scientific Reports · doi:10.1038/s41598-020-63962-0 · Cited by 10
Hallucination-Specific structure-function associations in schizophrenia
Roes, M., Yin, J., Taylor, L., Metzak, P. D., Lavigne, K. M., Chinchani, A. M., Tipper, C. M., & Woodward, T. S. (2020) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2020.111171 · Cited by 9
Characteristics of the corpus callosum in chronic schizophrenia treated with clozapine or risperidone and those never-treated
Bo, T., Xiao, Y., Cao, H., Zhang, W., Yang, C., Lencer, R., Gong, Q., & Lui, S. (2021) · BMC Psychiatry · doi:10.1186/s12888-021-03552-0 · Cited by 9
“Therefore, anatomical alterations in the anterior and midanterior region of the CC may be related to structural and functional abnormalities of the frontal lobe in schizophrenia, which generate delusions and hallucinations [26, 27].”
Background
The efficacy of low frequency repetitive transcial magnetic stimulation for treating auditory verbal hallucinations in schizophrenia: Insights from functional gradient analyses
Xie, Y., Li, C., Guan, M., Zhang, T., Ma, C., Wang, Z., Ma, Z., Wang, H., & Fang, P. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e30194 · Cited by 7
Hyper-Activated Brain Resting-State Network and Mismatch Negativity Deficit in Schizophrenia With Auditory Verbal Hallucination Revealed by an Event-Related Potential Evidence
Sun, Q., Fang, Y., Peng, X., Shi, Y., Chen, J., Wang, L., & Tan, L. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00765 · Cited by 8
High-Frequency Transcranial Random Noise Stimulation for Auditory Hallucinations of Schizophrenia: A Case Series
Mondino, M., Janin, D., Galvão, F., & Brunelin, J. (2022) · Biomedicines · doi:10.3390/biomedicines10112698 · Cited by 8
“montage was initially proposed based on the neurophysiological polarity-dependent properties of tDCS electrodes and neuroimaging studies demonstrating hyperactivity within temporoparietal areas and abnormal frontotemporal connectivity in patients with hallucinations [6,7].”
Method
Functional Connectivity Between Auditory and Medial Temporal Lobe Networks in Antipsychotic-Naïve Patients With First-Episode Schizophrenia Predicts the Effects of Dopamine Antagonism on Auditory Verbal Hallucinations
Anhøj, S. J., Ebdrup, B. H., Nielsen, M. Ø., Antonsen, P. K., Glenthoj, B. Y., & Rostrup, E. (2023) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2023.06.003 · Cited by 8
“First, in clinical studies, the hippocampal formation has been robustly linked to the pathophysiology of schizophrenia (28) and speci ﬁ cally to the development of auditory hallucinations (29).”
Background
Hypoactivation of the language network during auditory imagery contributes to hallucinations in Schizophrenia
Besso, L., Larivière, S., Roes, M., Sanford, N., Percival, C. M., Damascelli, M., Momeni, A., Lavigne, K. M., Menon, M., Aleman, A., et al. (2024) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2024.111824 · Cited by 10
“However, the LN is not normally separated from the STG network in most studies, but they are listed alongside one another, typically as hyperactive in hallucinations (Allen et al., 2008, 2012; ´ ˇ ´ et al., 2013; Jardri et al., 2011).”
Functional Neuroimaging of Hallucinations
Aleman, A., & Vercammen, A. (2011) · Springer eBooks · doi:10.1007/978-1-4614-0959-5_20 · Cited by 8
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Current Practice and New Developments in the Use of In Vivo Magnetic Resonance Spectroscopy for the Assessment of Key Metabolites Implicated in the Pathophysiology of Schizophrenia
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Auditory P300 as a Neurophysiological Correlate of Symptomatic Improvement by Transcranial Direct Current Stimulation in Patients With Schizophrenia: A Pilot Study
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“treatment of various symptoms in schizophrenia, by stimulating the hypofunctioning frontal cortex and suppressing the hyperfunctioning temporal cortex, has gained increasing attention.(10,11) Brunelin et al(12) were the first to perform a randomized controlled trial in which they reported an effect of tDCS not only on…”
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Review of Schizophrenia Research Using MEG
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Brain structure in schizophrenia: what do we know and what next?
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Authors: Jardri, R., Pouchet, A., Pins, D., & Thomas, P.
Affiliations: Centre National de la Recherche Scientifique (FR)
ORCID: Jardri, Renaud
Pins, Delphine
Thomas, Pierre
Venue: American Journal of Psychiatry
Publisher: American Psychiatric Association Publishing
Published: 2011-01
Volume: 168
Issue: 1
Pages: 73-81
ISSN: 0002-953X (ISSN-L)
1535-7228
DOI: 10.1176/appi.ajp.2010.09101522
OpenAlex: W2142837020
Cited by: 651
References: 99
Citations by year: 2026: 25 · 2025: 34 · 2024: 31 · 2023: 26 · 2022: 42 · 2021: 43 · 2020: 50 · 2019: 51 · 2018: 50 · 2017: 36 · 2016: 54 · 2015: 30 · 2014: 43 · 2013: 38 · 2012: 72
FWCI: 3.17
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Psychiatry (publishedVersion)
PubMed (publishedVersion)
HAL (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, schizophrenia spectrum disorders, cortical activation, activation likelihood estimation, Broca's area, anterior insula, frontal operculum, temporal lobe, hippocampus, parahippocampal region, speech generation, speech perception, verbal memory, fronto-temporal network, medial temporal lobe
MeSH terms: Brain Mapping, Cerebral Cortex, Hallucinations, Humans, Magnetic Resonance Imaging, Schizophrenia, Schizophrenic Psychology, Positron-Emission Tomography

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Cortical Activations During Auditory Verbal Hallucinations in Schizophrenia: A Coordinate-Based Meta-Analysis

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