Reality of auditory verbal hallucinations
Open accessAbstract
Distortion of the sense of reality, actualized in delusions and hallucinations, is the key feature of psychosis but the underlying neuronal correlates remain largely unknown. We studied 11 highly functioning subjects with schizophrenia or schizoaffective disorder while they rated the reality of auditory verbal hallucinations (AVH) during functional magnetic resonance imaging (fMRI). The subjective reality of AVH correlated strongly and specifically with the hallucination-related activation strength of the inferior frontal gyri (IFG), including the Broca's language region. Furthermore, how real the hallucination that subjects experienced was depended on the hallucination-related coupling between the IFG, the ventral striatum, the auditory cortex, the right posterior temporal lobe, and the cingulate cortex. Our findings suggest that the subjective reality of AVH is related to motor mechanisms of speech comprehension, with contributions from sensory and salience-detection-related brain regions as well as circuitries related to self-monitoring and the experience of agency.
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Raij et al. reported that subjective ratings of the reality of auditory/verbal hallucinations were positively correlated with enhanced coupling linking left inferior frontal gyrus to bilateral auditory cortices and posterior temporal lobes elicited by auditory/verbal hallucinations.
“Raij et al. reported that subjective ratings of the reality of AVHs were positively correlated with enhanced coupling linking left IFG to bilateral auditory cortices and posterior temporal lobes elicited by AVHs (67).”
From Elevated functional connectivity along a corticostriatal loop and the mechanism of auditory/verbal hallucinations in patients with schizophrenia (2011) · cites this paper as [67]
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“Interestingly, the experience that the auditory verbal hallucinations are a product of one's mind rather than real percepts may be associated with the involvement of the CMS during the hallucinations (Raij et al., 2009).”
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“Interestingly, an SMA lesion can cause alien limb syndrome, characterized by apparently purposeful, but unintended movements of the limb (Scepkowski and Cronin-Golomb, 2003).”
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The psychosis human connectome project: An overview
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“Psychosis is characterized by altered perceptual experiences (halucinations) and delusional beliefs that distort one’s sense of realty and, as a result, significantly impair a person’s ability to funcion in their social and occupational roles ( Raij et al., 2009 ).”
Electrophysiological correlates of retrieval orientation in reality monitoring
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“The role prefrontal brain structures in reality monitoring is also underlined by a recent fMRI study on schizophrenia patients with auditory verbal hallucinations (Raij et al., 2009).”
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Brainnetome-wide association studies in schizophrenia: The advances and future
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Authorship and Control over Thoughts
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“…neural basis of auditory hallucinations in schizophrenia has been extensively investigated (Silbersweig et al., 1995; Silbersweig and Stern, 1996; Epstein et al., 1999; Lennox et al., 2000; Raij et al., 2009; Jardri et al., 2011), the neurobiology of delusions has not been so well characterized.”
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Insights into hallucinations in schizophrenia: Novel treatment approaches
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Reduced glymphatic clearance in early psychosis
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“Individuals with psychosis typically experience distorted perceptual experiences, hallucinations, and delusional beliefs, signi fi cantly impacting the patient ’ s sense of reality [3, 4].”
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Auditory verbal hallucinations result from combinatoric associations of multiple neural events
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“However, another methodologically different fMRI study has shown that acoustic clarity was associated with activity in the inferior frontal gyri (Raij et al., 2009).”
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Psychology and Neurobiology of Horror Movies
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“, 2007) or auditory verbal hallucinations (AVH) experienced by schizophrenic patients (Hoffman et al., 2007; Raij et al., 2009).”
BackgroundHommes, J. E., A, L. K. M., Versmissen, D., Kircher, T. T. J., van Os, J., & van Winkel, R. (2011) · Psychological Medicine · doi:10.1017/s0033291711001152 · Cited by 18 · see citing works
“These studies reported both under- and overactivation associated with self-monitoring alterations (Shergill et al. 2000 ; Schnell et al. 2008 ; Raij et al. 2009), and these findings were hypothesized to result from a pathological increase in microstructural elements supporting excitatory neurotransmission, leading to…”
BackgroundCurtis, M. T., Coffman, B. A., & Salisbury, D. F. (2020) · Human Brain Mapping · doi:10.1002/hbm.25256 · Cited by 16 · see citing works
“…temporal lobe, and superior temporal gyrus ( Curči c-Blake et al., 2017; Dierks et al., 1999; Hoffman, 1986; Jardri, Pouchet, Pins, & Thomas, 2011; Raij et al., 2009), and gray matter deficits within the superior temporal gyrus are related to hallucinations in chronic schizophrenia (Asami et…”
BackgroundGörnerová, N., Brunovský, M., Klírová, M., Novák, T., Zaytseva, Y., Kopřivová, J., Bravermanová, A., & Horáček, J. (2022) · Neuroscience Letters · doi:10.1016/j.neulet.2022.136977 · Cited by 16 · see citing works
Sharaev, M., Малашенкова, И. К., Масленникова, А. В., Zakharova, N. V., Bernstein, A. V., Burnaev, E. V., Mamedova, G., Krynskiy, S., Ogurtsov, D., Kondrateva, E. A., et al. (2022) · Современные технологии в медицине · doi:10.17691/stm2022.14.5.06 · Cited by 17 · see citing works
Gao, J., Zhang, D.-S., Wang, L., Wang, W., Fan, Y.-J., Tang, M., Zhang, X., Lei, X.-Y., Wang, Y.-R., Yang, J., et al. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00575 · Cited by 16 · see citing works
Fuentes-Claramonte, P., Soler-Vidal, J., Salgado-Pineda, P., Garcia-Leon, M., Ramiro, N., Santo-Angles, A., Torres, M. L., Tristany, J., Guerrero-Pedraza, A., Munuera, J., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-98269-1 · Cited by 14 · see citing works
A working model of neural activity and phenomenal experience in psychosis
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“…to the secondary/associative auditory cortex) during auditory hallucinations is detectable in a consistent portion of patients [62, 63, 65, 70, 75, 76] and is speci fi cally related to increased phenomenal intensity (vividness and subjective reality) of the hallucinatory experience [75, 76].”
Xie, Y., Cai, Y., Guan, M., Wang, Z., Ma, Z., Fang, P., & Wang, H. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.971105 · Cited by 13 · see citing works
Agency and Ownership are Independent Components of ‘Sensing the Self’ in the Auditory-Verbal Domain
Hubl, D., Schneider, R. C., Kottlow, M., Kindler, J., Strik, W. K., Dierks, T., & Koenig, T. W. (2014) · Brain Topography · doi:10.1007/s10548-014-0351-0 · Cited by 11 · see citing works
“In an interesting study in hallucinating schizophrenia patients, exactly these cingulate regions exhibited a negative correlation between the hallucination-related coupling of the left inferior frontal gyrus and the posterior and rostral anterior cingulate cortex in dependency of the reality of auditory hallucinations…”
BackgroundFreitas, C., PEARLMAN, C. A., & Pascual‐Leone, Á. (2011) · Neurocase · doi:10.1080/13554794.2010.547864 · Cited by 11 · see citing works
“Recently, Raij et al. (2009 ) showed that the subjective reality of AVH is significantly and strongly related to activation of bilateral inferior frontal gyrus (IFG), rather than to any AVH-related activation in the temporal lobe (including the auditory cortices).”
BackgroundPanikratova, Y., Lebedeva, I., Akhutina, T., Tikhonov, D., Kaleda, V. G., & Vlasova, R. (2023) · Schizophrenia Research · doi:10.1016/j.schres.2023.10.026 · Cited by 10 · see citing works
Salisbury, D. F., Seebold, D., Longenecker, J., Coffman, B. A., & Yeh, F.-C. F. (2023) · Schizophrenia Research · doi:10.1016/j.schres.2023.06.001 · Cited by 8 · see citing works
Functional Neuroimaging of Hallucinations
Aleman, A., & Vercammen, A. (2012) · Springer eBooks · doi:10.1007/978-1-4614-0959-5_20 · Cited by 9 · see citing works
Connors, M. H., Robidoux, S., Langdon, R. A., & Coltheart, M. (2016) · Consciousness and Cognition · doi:10.1016/j.concog.2016.05.001 · Cited by 8 · see citing works
Conring, F., Gangl, N., Derome, M., Wiest, R., Federspiel, A., Walther, S., & Stegmayer, K. (2023) · NeuroImage: Clinical · doi:10.1016/j.nicl.2023.103527 · Cited by 7 · see citing works
“…et al., 2003; Hoffman et al., 2008; Lennox et al., 2000; Raij et al., 2009; Silbersweig et al., 1995; Sommer et al., 2008), ventral striatum (Raij et al., 2009), nucleus accumbens (Raij et al., 2009), thalamus (Lennox et al., 2000; Shergill et al., 2000; Sil-bersweig et al., 1995; Zmigrod…”
BackgroundInfluentialStructural aging of human neurons is opposite of the changes in schizophrenia
Mizutani, R., Saiga, R., Yamamoto, Y., Uesugi, M., Takeuchi, A., Uesugi, K., Terada, Y., Suzuki, Y., Andrade, V. D., Carlo, F. D., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0287646 · Cited by 5 · see citing works
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Activation of the motivation-related ventral striatum during delusional experience
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Connectivity Issues of the ‘Hallucinating’ Brain
Benetti, S., Pettersson‐Yeo, W., & Mechelli, A. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4121-2_22 · Cited by 5 · see citing works
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Dysconnectivity in Hallucinations
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Toward Molecular Psychotherapy of Depression?
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Neurocognitive Models of Auditory Verbal Hallucinations in Schizophrenia: A Review.
Panikratova, Y. R., & Лебедева, И. С. (2022) · Clinical Psychology and Special Education · doi:10.17759/cpse.2022110105 · Cited by 2 · see citing works
“The subjective reality of voices in patients with schizophrenia spectrum disorders is correlated with the functional connectivity of the inferior frontal gyrus with temporal regions and the anterior cingulate cortex [54].”
BackgroundEsse est percipi: A Neurophilosophical Model of Psychosis
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Auditory Verbal Hallucinations in Schizophrenia: A Model for Aberrant Self-consciousness
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“Therefore, there is a need to develop approaches that are designed to examine the brain network dysfunction underlying the experience of AVH using appropriately designed paradigms in selected individuals with schizophrenia having continuous AVH.”
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- Authors
- Raij, T. T., Valkonen-Korhonen, M., Holi, M., Therman, S., Lehtonen, J., & Hari, R.
- Affiliations
- University of Helsinki (FI)
- Kellokoski Hospital (FI)
- Kuopio University Hospital (FI)
- Helsinki University Hospital (FI)
- Corresponding author
- Raij, Tuukka T.
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2009-07-20
- Volume
- 132
- Issue
- 11
- Pages
- 2994-3001
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC2768657
- OpenAlex
- W1993041042
- Cited by
- 95
- References
- 55
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 9 · 2021: 4 · 2020: 5 · 2019: 5 · 2018: 5 · 2017: 5 · 2016: 5 · 2015: 7 · 2014: 11 · 2013: 5 · 2012: 8
- FWCI
- 3.71
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Brain (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
- Funders
- Suomen Lääketieteen Säätiö
- Jalmari ja Rauha Ahokkaan Säätiö
- Academy of Finland
- Ella ja Georg Ehrnroothin Säätiö
- FP7 Ideas: European Research Council (232946)
- 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, schizoaffective disorder, inferior frontal gyrus, Broca's area, ventral striatum, auditory cortex, posterior temporal lobe, cingulate cortex, speech understanding, self-monitoring, sense of agency, saliency detection, psychosis
- MeSH terms
- Adult, Auditory Pathways, Auditory Perception, Brain Mapping, Cerebral Cortex, Female, Hallucinations, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Nerve Net, Psychotic Disorders, Schizophrenia, Speech Perception, Young Adult
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