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Cortical Activations During Auditory Verbal Hallucinations in Schizophrenia: A Coordinate-Based Meta-Analysis
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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“Our present study extends this by showing commonalities between many of the neural regions activated during AVH (such as left STG, left insula, left IFG) and those strongly activated during dialogic inner speech (Jardri et al., 2011; Kühn and Gallinat, 2012).”
From The brain's conversation with itself: neural substrates of dialogic inner speech (2016) · cites this paper as Jardri et al., 2011
In the citing paper
“Recent meta-analyses of symptom-capture studies have come to only partially overlapping conclusions: while Jardri et al. (2011) found AVHs to be associated with activation in left IFG, anterior insula, superior temporal, and hippocampal areas, Kühn and Gallinat (2012) could only find consistent results for bilateral IFG, postcentral gyrus, and parietal areas.”
From Inner Speech: Development, Cognitive Functions, Phenomenology, and Neurobiology (2015) · cites this paper as Jardri et al. (2011)
In the citing paper
“Increased activation within a bilateral frontotemporal network was confirmed by coordinate-based metaanalysis of the auditory hallucination (AH) state.27”
From Are hallucinations due to an imbalance between excitatory and inhibitory influences on the brain? (2016) · cites this paper as [27]
Citations
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Cited by
Sorted by citations
Large-scale brain networks and psychopathology: a unifying triple network model
Menon, V. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.08.003 · Cited by 4,168
Inner Speech: Development, Cognitive Functions, Phenomenology, and Neurobiology
Alderson-Day, B., & Fernyhough, C. (2015) · Psychological Bulletin · doi:10.1037/bul0000021 · Cited by 864
“Recent meta-analyses of symptomcapture studies have come to only partially overlapping conclusions: while Jardri et al. (2011) found AVHs to be associated with activation in left IFG, anterior insula, superior temporal, and hippocampal areas, Kühn and Gallinat (2012) could only find consistent…”
ResultFregni, F., El-Hagrassy, M. M., Pacheco‐Barrios, K., Carvalho, S., Leite, J., Simis, M., Brunelin, J., Nakamura-Palacios, E. M., Marangolo, P., Venkatasubramanian, G., et al. (2020) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaa051 · Cited by 654
Hallucinations and strong priors
Corlett, P. R., Horga, G., Fletcher, P. C., Alderson-Day, B., Schmack, K., & Powers, A. R. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.12.001 · Cited by 534
“Critically, the neural circuit underlying these conditioned phenomena, including superior temporal gyrus and insula, largely overlapped with the circuit engaged when patients report hearing voices in the scanner [34,35].”
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Metadata
- Authors
- Jardri, R., Pouchet, A., Pins, D., & Thomas, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Venue
- American Journal of Psychiatry
- Published
- 2011-01
- Volume
- 168
- Issue
- 1
- Pages
- 73-81
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- 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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