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Interaction of language, auditory and memory brain networks in auditory verbal hallucinations
Open accessAbstract
Auditory verbal hallucinations (AVH) occur in psychotic disorders, but also as a symptom of other conditions and even in healthy people. Several current theories on the origin of AVH converge, with neuroimaging studies suggesting that the language, auditory and memory/limbic networks are of particular relevance. However, reconciliation of these theories with experimental evidence is missing. We review 50 studies investigating functional (EEG and fMRI) and anatomic (diffusion tensor imaging) connectivity in these networks, and explore the evidence supporting abnormal connectivity in these networks associated with AVH. We distinguish between functional connectivity during an actual hallucination experience (symptom capture) and functional connectivity during either the resting state or a task comparing individuals who hallucinate with those who do not (symptom association studies). Symptom capture studies clearly reveal a pattern of increased coupling among the auditory, language and striatal regions. Anatomical and symptom association functional studies suggest that the interhemispheric connectivity between posterior auditory regions may depend on the phase of illness, with increases in non-psychotic individuals and first episode patients and decreases in chronic patients. Leading hypotheses involving concepts as unstable memories, source monitoring, top-down attention, and hybrid models of hallucinations are supported in part by the published connectivity data, although several caveats and inconsistencies remain. Specifically, possible changes in fronto-temporal connectivity are still under debate. Precise hypotheses concerning the directionality of connections deduced from current theoretical approaches should be tested using experimental approaches that allow for discrimination of competing hypotheses.
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“In addition, evidence supports the hypothesis that hallucinations arise from release of those sensory signals by reduced top-down inhibition from higher-order centers such as frontal areas and their connections with the thalamus. 40-43”
From Towards an Integrative Account of Potential Mechanisms Mediating the Path From Sleep Dysfunction to Hallucinations (2025) · cites this paper as [41]
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Alamian, G., Pascarella, A., Lajnef, T., Knight, L., Walters, J., Singh, K. D., & Jerbi, K. (2020) · NeuroImage Clinical · doi:10.1016/j.nicl.2020.102485 · Cited by 16
“, 1994; Uhlhaas and Singer, 2010) have probed structural and functional alterations among schizophrenia patients and have found significant and consistent differences in terms of the physical properties and connectivity patterns of their neural signal compared to controls (multimodal reviews: Alamian et al., 2017; Ćur…”
Richards, S., Hughes, M., Woodward, T., Rossell, S., & Carruthers, S. (2021) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.006 · Cited by 14
Cheng Ann, C. H. E. N., Huang, H., Qin, X., Zhang, L., Rong, B., Wang, G., & Wang, H. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.956895 · Cited by 16
Zhuo, C., Zhou, C., Lin, X., Tian, H., Wang, L., Chen, C., Ji, F., Xu, Y. J., & Jian, D. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109738 · Cited by 16
Weber, S., Hjelmervik, H., Craven, A., Johnsen, E., Kroken, R., Løberg, E., Ersland, L., Kompus, K., & Hugdahl, K. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.643564 · Cited by 17
“Based on findings of impaired cognitive control in patients with AVH during an auditory task (33) as well as abnormal connectivity between the ACC and the STG (2), it has been suggested that AVH arise from impaired top-down control of prefrontal areas over bottom-up processes in auditory areas (2, 22, 29).”
BackgroundSun, Q., Fang, Y., Shi, Y., Wang, L., Peng, X., & Tan, L. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.544746 · Cited by 16
Liang, N., Liu, S., Li, X.-R., Wen, D., Li, Q.-Q., Tong, Y., & Xu, Y. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.865738 · Cited by 15
Gill, K., Percival, C. M., Roes, M., Arreaza, L., Chinchani, A. M., Sanford, N., Sena, W., Mohammadsadeghi, H., Menon, M., Hughes, M. E., et al. (2022) · Schizophrenia Bulletin Open · doi:10.1093/schizbullopen/sgac050 · Cited by 19
“Component 3 is characterized by bilateral deactivation in occipital areas such as the occipital pole (xyz: −27, −91, 16; 15, −88, 28).”
BackgroundGao, J., Zhang, D., Wang, L., Wang, W., Fan, Y., Tang, M., Zhang, X., Lei, X., Wang, Y., Yang, J., et al. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00575 · Cited by 17
“In previous models including the “memory intrusion”, “selfmonitoring”, “two hit bottom-up and top-down”, and hybrid models, language, auditory, and memory brain networks were closely associated with AVH in patients with schizophrenia (4).”
BackgroundOkuneye, V. T., Meda, S., Pearlson, G., Clementz, B., Keshavan, M., Tamminga, C., Ivleva, E., Sweeney, J., Gershon, E., & Keedy, S. (2020) · NeuroImage: Clinical · doi:10.1016/j.nicl.2020.102358 · Cited by 14
“The models include hypersensitivity or activation of auditory cortex including primary and association auditory cortex, and/or adjacent polymodal association cortex of the inferior parietal lobe, dysregulation of receptive auditory cortex by disrupted top-down influences especially from frontal speech areas, altered i…”
Strawson, W., Wang, H.-T., Quadt, L., Sherman, M. T., Larsson, D. E. O., Davies, G., Mckeown, B., Silva, M., Fielding-Smith, S. F., Bibby-Jones, A.-M., et al. (2021) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyab093 · Cited by 14
“Symptom-capture studies of AVH echo the involvement of temporal language regions: meta-analyses support greater activation in STG and adjacent temporo-parietal language regions during AVH experience in patients with schizophrenia (Ćurčić-Blake et al., 2017).”
BackgroundMethodUncovering hidden resting state dynamics: A new perspective on auditory verbal hallucinations
Honcamp, H., Schwartze, M., Linden, D. E. J., El‐Deredy, W., & Kotz, S. A. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119188 · Cited by 12
“The altered FC between IFG and parahippocampal regions in non-clinical voice-hearers might facilitate memory retrieval, thereby providing additional evidence for the hypothesized intrusion of long-term memory into ongoing cognitive processes (Ćurčić-Blake et al., 2017; Diederen et al., 2012).”
BackgroundAn integrative perspective on the role of touch in the development of intersubjectivity
Plinio, S. D., Scalabrini, A., & Ebisch, S. J. H. (2022) · Brain and Cognition · doi:10.1016/j.bandc.2022.105915 · Cited by 15
Draining the pond and catching the fish: Uncovering the ecosystem of auditory verbal hallucinations
Looijestijn, J., Blom, J. D., Hoek, H. W., Renken, R. J., Liemburg, E. J., Sommer, I. E., Aleman, A., & Goekoop, R. (2018) · NeuroImage Clinical · doi:10.1016/j.nicl.2018.09.016 · Cited by 13
Zhuo, C., Li, G., Ji, F., Chen, C., Jiang, D., Lin, X., Xu, Y. J., Tian, H., Wang, L., Zhou, C., et al. (2020) · Brain Imaging and Behavior · doi:10.1007/s11682-019-00210-8 · Cited by 13
“In recent years, based on studies of AVH and NVAH in patients with schizophrenia, many researchers have proposed that AVH are caused by disturbances in brain circuits and networks (Curcic-Blake et al. 2017).”
BackgroundChen, Y., Guo, Z., Wang, Y., Yin, H., Zhang, S., & Liu, W. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1102927 · Cited by 12
“The STG processes auditory signals from the primary auditory cortex and then via the thalamus sends them to higher-order areas and other language areas (33).”
BackgroundInteractive mapping of language and memory with the GE2REC protocol
Banjac, S., Roger, É., Cousin, É., Perrone‐Bertolotti, M., Haldin, C., Pichat, C., Lamalle, L., Minotti, L., Kahane, P., & Baciu, M. (2020) · Brain Imaging and Behavior · doi:10.1007/s11682-020-00355-x · Cited by 12
“Furthermore, there are disorders such as post-stroke aphasia (Schuchard and Thompson 2014) or conditions that cause auditory hallucinations ( Ć ur č i ć -Blake et al. 2017) in which language regions are impaired, but the symptoms also manifest in the memory domain.”
BackgroundHe, J., Ren, H., Li, J., Dong, M., Dai, L., Li, Z., Miao, Y., Li, Y., Tan, P., Gu, L., et al. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.831714 · Cited by 12
Altered language network lateralization in euthymic bipolar patients: a pilot study
Romeo, Z., Marino, M., Angrilli, A., Semenzato, I., Favaro, A., Magnolfi, G., Padovan, G. B., Mantini, D., & Spironelli, C. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02202-7 · Cited by 12
“At the same time, past findings suggested that AVH are associated with increased connectivity among inferior frontal gyrus, Wernicke’s area, and striatal brain regions, also distributed to right hemisphere homologs [72].”
BackgroundRieger, K., Rarra, M.-H., Hernandez, L. D., Hubl, D., & Koenig, T. W. (2018) · Clinical EEG and Neuroscience · doi:10.1177/1550059418765810 · Cited by 12
“6 In the first pre-session (1), patients were fully informed about the experimental procedure and inclusion and exclusion criteria were evaluated.”
MethodFalkenberg, L. E., Westerhausen, R., Johnsen, E., Kroken, R., Løberg, E., Bereśniewicz, J., Kazimierczak, K., Kompus, K., Ersland, L., Sandøy, L. B., et al. (2020) · Psychiatry research. Neuroimaging · doi:10.1016/j.pscychresns.2020.111088 · Cited by 11
Hwang, M., Roh, Y. S., Talero, J., Cohen, B. M., Baker, J. T., Brady, R. O., Öngür, D., & Shinn, A. K. (2021) · NeuroImage Clinical · doi:10.1016/j.nicl.2021.102893 · Cited by 15
Zhuo, C., Ji, F., Lin, X. J., Tian, H., Wang, L., Xu, Y. J., Wang, W., Zhong, B., & Lin, X. (2020) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-020-01102-5 · Cited by 11
“In summary, our findings of this pilot study are more inclined to support the “imbalance in top-down/bottom-up influences” hypothesis of AVH [35, 41, 43, 45].”
BackgroundResultInfluentialFrancis, A. M., Knott, V., Labelle, A., & Fisher, D. J. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.540738 · Cited by 11
“It has been previously shown that AHs are reduced when external speech is present (20–22), with a corresponding deactivation of auditory cortex suggesting generalized cortical hypofunction due to sensory overload when AHs compete with external auditory stimulation (98, 99).”
BackgroundCircular inference predicts nonuniform overactivation and dysconnectivity in brain-wide connectomes
Bouttier, V., Duttagupta, S., Denève, S., & Jardri, R. (2021) · Schizophrenia Research · doi:10.1016/j.schres.2020.12.045 · Cited by 14
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
Zhuo, C., Tian, H., Fang, T., Li, R., Li, Y., Kong, L., Cai, Z., Zheng, L., Lin, X., & Chen, C. (2020) · Europe PMC (PubMed Central) · Cited by 9
Bereśniewicz, J., Craven, A., Hugdahl, K., Løberg, E., Kroken, R., Johnsen, E., & Grüner, R. (2021) · Diagnostics · doi:10.3390/diagnostics11010139 · Cited by 8
“Several studies suggest that the left arcuate fasciculus, which is the critical pathway of the language network, show reduced FA-values in AVH+ patients [6,17,61,62].”
BackgroundResultAubonnet, R., Banea, O. C., Sirica, R., Wassermann, E. M., Yassine, S., Jacob, D., Magnúsdóttir, B. B., Haraldsson, M. H., Stefánsson, S. B., Jónasson, V. D., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.575538 · Cited by 9
Hu, J.-H., Xǔ, J., Shang, S., Chen, H., Yin, X., Qi, J., & Wu, Y. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.752419 · Cited by 10
Metadata
- Authors
- Ćurčić-Blake, B., Ford, J. M., Hubl, D., Orlov, N. D., Sommer, I. E., Waters, F., Allen, P., Jardri, R., Woodruff, P. W., David, O., Mulert, C., Woodward, T. S., & Aleman, A.
- Affiliations
- San Francisco VA Medical Center (US)
- University of Bern (CH)
- King's College London (GB)
- University Medical Center Utrecht (NL)
- The University of Western Australia (AU)
- Centre National de la Recherche Scientifique (FR)
- University of Sheffield (GB)
- University Medical Center Hamburg-Eppendorf (DE)
- University of British Columbia (CA)
- University Medical Center Groningen (NL)
- ORCID
- Venue
- Progress in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2017-01
- Volume
- 148
- Pages
- 1-20
- ISSN
- 0301-0082 (ISSN-L)
- PMC
- PMC5240789
- OpenAlex
- W2552561399
- Cited by
- 224
- References
- 200
- Citations by year
- 2026: 13 · 2025: 21 · 2024: 20 · 2023: 18 · 2022: 21 · 2021: 28 · 2020: 34 · 2019: 35 · 2018: 20 · 2017: 13
- FWCI
- 2.43
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Progress in Neurobiology (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by-nc-nd)
- HAL (submittedVersion, cc-by-nc-nd)
- UWA Profiles and Research Repository (UWA) (submittedVersion, cc-by-nc-nd)
- BORIS (University Library Bern) (submittedVersion, cc-by-nc-nd)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Research Portal (King's College London) (submittedVersion, cc-by-nc-nd)
- LillOA (Université de Lille (University Of Lille)) (submittedVersion, cc-by-nc-nd)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by-nc-nd)
- Open Access CRIS of the University of Bern
- Funders
- NWO VICI (453-11-004)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Hallucinations in medical conditions
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- auditory verbal hallucinations, language network, auditory network, functional connectivity, structural connectivity, symptom association, interhemispheric connectivity, striatum, source monitoring, top-down attention, psychosis, first-episode psychosis, chronic psychosis, fronto-temporal connectivity
- MeSH terms
- Auditory Perception, Hallucinations, Humans, Language, Memory, Nerve Net
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