Cited by 579Hallucinations in medical conditionsSchizophrenia research and treatmentVisual perception and processing mechanisms

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The hallucinating brain: A review of structural and functional neuroimaging studies of hallucinations

Allen, Paul, Larøi, Frank, McGuire, Philip K., Aleman, Andrè·2008·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2007.07.012

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Abstract

Hallucinations remains one of the most intriguing phenomena in psychopathology. In the past two decades the advent of neuroimaging techniques have allowed researchers to investigate what is happening in the brain of those who experience hallucinations. In this article we review both structural and functional neuroimaging studies of patients with auditory and visual hallucinations as well as a small number of studies that have assessed cognitive processes associated with hallucinations in healthy volunteers. The current literature suggests that in addition to secondary (and occasionally primary) sensory cortices, dysfunction in prefrontal premotor, cingulate, subcortical and cerebellar regions also seem to contribute to hallucinatory experiences. Based on the findings of these studies we tentatively propose a neurocognitive model in which both bottom-up and top-down processes interact to produce these erroneous percepts. Finally, directions for future work are discussed.

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“recent findings [5], [6], the substantial similarity between the hallucinations and real voices is connected to alterations in a brain network related to speech and language processing.”
Background
Common mechanisms of auditory hallucinations–perfusion studies in epilepsy
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Background
The Static and dynamic functional connectivity characteristics of the left temporoparietal junction region in schizophrenia patients with auditory verbal hallucinations during low-frequency rTMS treatment
Xie, Y.-J., Guan, M.-Z., He, Y., Wang, Z.-H., Ma, Z.-J., Fang, P., & Wang, H.-N. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1071769 · Cited by 20
“Left TPJ as a critical stimulation target implicated in AVH generation and perception (3, 48).”
Background
Metabolite differences in the medial prefrontal cortex in schizophrenia patients with and without persistent auditory verbal hallucinations: a 1H MRS study
Wang, Q., Ren, H., Li, C., Li, Z., Li, J., Li, H., Dai, L., Dong, M., Zhou, J., He, J., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01866-5 · Cited by 18
Misattribution Models (II): Source Monitoring in Hallucinating Schizophrenia Subjects
Woodward, T. S., & Menon, M. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4121-2_10 · Cited by 21
“Relative to the strong evidence for the over-perceptualization account of hallucinations, direct evidence for degraded top-down “generating-thoughts” signal is lacking, and top-down dysfunction is considered secondary to bottom-up overactivity (Allen et al., 2008).”
BackgroundInfluential
Risk factors for visual hallucinations in patients with Parkinson’s disease
Gama, R. L., de Bruin, V. M. S., de Bruin, P. F. C., Távora, D. G. F., Lopes, E. M. S., Jorge, I. F., Bittencourt, L., & Tufik, S. B. (2014) · Neurological Research · doi:10.1179/1743132814y.0000000418 · Cited by 17
Structural Associations of Cortical Contrast and Thickness in First Episode Psychosis
Makowski, C., Lewis, J. D., Lepage, C., MALLA, A. K., Joober, R., Lepage, M., & Evans, A. C. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz040 · Cited by 17
Implications from translational cross-validation of clinical assessment tools for diagnosis and treatment in psychiatry
Aryutova, K., Paunova, R., Kandilarova, S., Todeva-Radneva, A., & Stoyanov, D. (2021) · World Journal of Psychiatry · doi:10.5498/wjp.v11.i5.169 · Cited by 18
External speech processing and auditory verbal hallucinations: A systematic review of functional neuroimaging studies.
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
A preliminary study to investigate resting state fMRI as a potential group differentiator for schizophrenia
Goswami, S., Beniwal, R. P., Kumar, M., Triptish Bhatia, A., Gur, R. E., Gur, R. C., Khushu, S., & Deshpande, S. N. (2020) · Asian Journal of Psychiatry · doi:10.1016/j.ajp.2020.102095 · Cited by 17
Computational Models of Hallucinations
Jardri, R., & Denève, S. (2013) · The Neuroscience of Hallucinations · doi:10.1007/978-1-4614-4121-2_16 · Cited by 16
The effect of low-frequency rTMS on auditory hallucinations, EEG source localization and functional connectivity in schizophrenia
Görnerová, 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
A two-factor structure of first rank symptoms in patients with a psychotic disorder
Heering, H. D., van Haren, N. E. M., & Derks, E. M. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.04.032 · Cited by 16
“Research on potential mechanisms underlying FRS-auditory hallucinations suggest that specific anomalies in speech production and speechmonitoring brain areasmight be responsible (Allen et al., 2008; Fisher et al., 2008; Daalman et al., 2011).”
Common and Distinct Alterations of Cognitive Function and Brain Structure in Schizophrenia and Major Depressive Disorder: A Pilot Study
Ma, M., Zhang, Y., Zhang, X., Yan, H., Zhang, D., & Yue, W. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.705998 · Cited by 16
Multimodal morphometry and functional magnetic resonance imaging in schizophrenia and auditory hallucinations
García‐Martí, G. (2012) · World Journal of Radiology · doi:10.4329/wjr.v4.i4.159 · Cited by 16
A Lacanian perspective on psychotic hallucinations
Vanheule, S. (2011) · Theory & Psychology · doi:10.1177/0959354310369275 · Cited by 15
“An extensive network of cortical and subcortical areas thereby proved to be activated during hallucinatory activity, ranging from speech production and speech reception areas, to monitoring areas, association areas, and areas involved in emotion regulation and attention (Allen et al., 2007; Allen et al., 2008; Tracy &…”
Background
Real-Time Symptom Capture of Hallucinations in Schizophrenia with fMRI: Absence of Duration-Dependent Activity
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
“16 Metacognitive or belief-based influences are also likely play a role 17–19 ; therefore, a network-based approach is important for investigating the biological underpinnings of hallucinations.”
Background
Diagnosis of Schizophrenia Based on the Data of Various Modalities: Biomarkers and Machine Learning Techniques (Review)
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 22
“beyond the speech zones, are closely connected with the occurrence of auditory hallucinations [51].”
Background
Spatiotemporal dynamics of functional connectivity and association with molecular architecture in schizophrenia
Hou, C., Jiang, S., Liu, M., Li, H., Zhang, L., Duan, M., Yao, G., He, H., Yao, D., & Luo, C. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad185 · Cited by 15
Neurological soft signs (NSS) and brain morphology in patients with chronic schizophrenia and healthy controls
Herold, C. J., Essig, M., & Schröder, J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0231669 · Cited by 15
Altered Functional Connectivity of the Nucleus Accumbens Network Between Deficit and Non-deficit Schizophrenia
Zhou, C., Xue, C., Chen, J., Amdanee, N., Tang, X., Zhang, H., Zhang, F., Zhang, X., & Zhang, C. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.704631 · Cited by 15
A case of persistent visual hallucinations of faces following LSD abuse: A functional Magnetic Resonance Imaging study
Iaria, G., Fox, C. J., Scheel, M., Stowe, R., & Barton, J. J. S. (2009) · Neurocase · doi:10.1080/13554790903329141 · Cited by 15
“While our data agree with the majority of studies showing increased BOLD signal changes in many visual and non-visual areas during hallucinatory periods ( Allen, Laroi, McGuire, & Aleman, 2008 ; Ffytche et al, 1998 ; Silbersweig et al, 1995 ) ( Figure 1 ), they provide the new observation that during hallucinations de…”
Result
Consciousness and Hallucinations in Schizophrenia: The Role of Synapse Regression
Ao, M. R. B. (2008) · Australian & New Zealand Journal of Psychiatry · doi:10.1080/00048670802419253 · Cited by 16
“Studies with fMRI show that in schizophrenia not only is the primary auditory cortex in Heschl’s gyrus active, as it is in auditory illusions, but also the auditory cortical areas in the superior temporal gyrus [46] (for a review see [40]).”
Integrative etiopathogenetic models of psychotic disorders: methods, evidence and concepts
Gaebel, W., & Zielasek, J. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr078 · Cited by 14
Resting state auditory-language cortex connectivity is associated with hallucinations in clinical and biological subtypes of psychotic disorders
Okuneye, 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…”
Aberrant Perceptual Judgments on Speech-Relevant Acoustic Features in Hallucination-Prone Individuals
Erb, J., Kreitewolf, J., Pinheiro, A. P., & Obleser, J. (2020) · Schizophrenia Bulletin Open · doi:10.1093/schizbullopen/sgaa059 · Cited by 15
Network analysis of psychiatric symptoms in schizophrenia: Findings from the Research on Asian Psychotropic Prescription Patterns for Antipsychotics (REAP-AP)
Li, W., Zhang, Q., Tang, Y., Park, S., Park, Y. C., Yang, S., Chen, L., Lin, S., Najoan, E., Kallivayalil, R. A., et al. (2022) · Asian Journal of Psychiatry · doi:10.1016/j.ajp.2022.103200 · Cited by 14
A Mini Review on the Contribution of the Anterior Cingulate Cortex in the Risk of Psychosis in 22q11.2 Deletion Syndrome
Padula, M. C., Scariati, E., Schaer, M., & Eliez, S. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00372 · Cited by 15
Auditory processing deficits in bipolar disorder with and without a history of psychotic features
Zenisek, R., Thaler, N. S., Sutton, G. P., Ringdahl, E. N., Snyder, J. S., & Allen, D. N. (2015) · Bipolar Disorders · doi:10.1111/bdi.12333 · Cited by 14
“The mechanisms underlying auditory hallucinations are not completely clear, and structural and functional abnormalities in multiple brain structures have been implicated [for a review, see (24)], suggesting that auditory hallucinations may be associated with dysfunction in a functional network of brain regions.”
Background
Subcomponents of brain T2* relaxation in schizophrenia, bipolar disorder and siblings: A Gradient Echo Plural Contrast Imaging (GEPCI) study
Mamah, D. T., Wen, J., Luo, J., Ulrich, X., Barch, D. M., & Yablonskiy, D. A. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.10.004 · Cited by 14
“Dysfunction of either the STG of its network of connections is pertinent to SCZ and has been closely linked to two key positive symptoms, auditory hallucinations and thought disorder (Allen et al., 2008; Pearlson, 1997; Shenton et al., 1992).”
Voice Hearing in Borderline Personality Disorder Across Perceptual, Subjective, and Neural Dimensions
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
“…of AVH in patients with schizophrenia: AVH are linked to multiple functional alterations (Ćurčić-Blake et al., 2017) yet most consistently with hyperactivity in language-related temporal lobe regions (Allen et al., 2008; Jardri et al., 2011; Kühn and Gallinat, 2012; Orlov et al., 2018).”
Background
Cortical thickness abnormalities in patients with first episode psychosis: a meta-analysis of psychoradiologic studies and replication in an independent sample
Wen, K., Zhao, Y., Gong, Q., Zhu, Z., Li, Q., Pan, N., Fu, S., Raduà, J., Vieta, E., Kumar, P., et al. (2021) · Psychoradiology · doi:10.1093/psyrad/kkab015 · Cited by 13
“The STC is thought to contain the auditory association cortical areas (Sun et al., 2009) and is a potential candidate for the neural basis of auditory hallucinations in psychosis (Allen et al., 2008).”
Neurofunctional assessment in a stroke patient with musical hallucinations
Calabrò, R. S., Baglieri, A., Ferlazzo, E., Passari, S., Marino, S., & Bramanti, P. (2012) · Neurocase · doi:10.1080/13554794.2011.633530 · Cited by 13
“fMRI studies showed that hallucinations in a given modality involve areas that normally process sensory information in that modality ( Allen, Laroi, McGuire, & Aleman, 2008 ; Kasai, Asada, Yumoto, Takeya, & Matsuda, 1999 ).”
Background
The Cortical Hyperexcitability Index (CHi): a new measure for quantifying correlates of visually driven cortical hyperexcitability
Braithwaite, J. J., Marchant, R., Takahashi, C., Dewe, H., & Watson, D. G. (2015) · Cognitive Neuropsychiatry · doi:10.1080/13546805.2015.1040152 · Cited by 13
“Simple elementary and complex hallucinatory experiences are associated with a range of conditions and disorders - which are, almost without exception, associated with cortically mediated aberrant neurophysiological activity (Aleman & Vercammen, 2012; Allen et al., 2008; Bien et al., 2000; Braun et al., 2003; Elliot et…”
Background
Repetition of letter strings leads to activation of and connectivity with word-related regions
Fisher, J. E., Cortes, C. R., Griego, J. A., & Tagamets, M. A. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.047 · Cited by 15
“These regions have been implicated in an inner speech network (Allen et al., 2008), and since the control task is also likely to involve inner speech, contrasts between the control and words conditions may not show activation differences in these regions.”
Background
Attentional Modulation of Source Attribution in First-Episode Psychosis: A Functional Magnetic Resonance Imaging Study
Kambeitz‐Ilankovic, L., Hennig‐Fast, K., Benetti, S., Kambeitz, J. P., Pettersson‐Yeo, W., O’Daly, O., McGuire, P. K., & Allen, P. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs101 · Cited by 13
Separating Mental Disorders Using Vestibular Field Potentials
Maller, J. J., Alfred, M., Gurvich, C., Haghgooie, S., Pouya, O. R., Fitzgerald, P. B., & Kulkarni, J. (2014) · Archives of Neuroscience · doi:10.5812/archneurosci.19257 · Cited by 13
Hypnosis in palliative care: from clinical insights to the science of self-regulation
Landry, M., Stendel, M. S., Landry, M., & Raz, A. (2018) · Annals of Palliative Medicine · doi:10.21037/apm.2017.12.05 · Cited by 14
Cortical thickness abnormalities in bipolar disorder patients with a lifetime history of auditory hallucinations
Mørch-Johnsen, L. E., Nerland, S., Jørgensen, K. N., Osnes, K., Hartberg, C. B., Andreassen, O. A., Melle, I. S., Nesvåg, R., & Agartz, I. (2018) · Bipolar Disorders · doi:10.1111/bdi.12627 · Cited by 12
Less reduced gray matter volume in the subregions of superior temporal gyrus predicts better treatment efficacy in drug-naive, first-episode schizophrenia
Cui, X., Deng, Q., Lang, B., Su, Q., Liu, F., Zhang, Z., Chen, J., Zhao, J., & Guo, W. (2020) · Brain Imaging and Behavior · doi:10.1007/s11682-020-00393-5 · Cited by 12
BNST and amygdala connectivity are altered during threat anticipation in schizophrenia
Feola, B., McHugo, M., Armstrong, K., Noall, M. P., Flook, E. A., Woodward, N. D., Heckers, S., & Blackford, J. U. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113428 · Cited by 12

Authors: Allen, P., Larøi, F., McGuire, P. K., & Aleman, A.
Affiliations: King's College London (GB)
University of Liège (BE)
University of London (GB)
Corresponding author: Allen, Paul
ORCID: Allen, Paul
Larøi, Frank
McGuire, Philip K.
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2008-01
Volume: 32
Issue: 1
Pages: 175-191
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2007.07.012
OpenAlex: W2107394985
Cited by: 579
References: 104
Citations by year: 2026: 20 · 2025: 20 · 2024: 21 · 2023: 54 · 2022: 32 · 2021: 32 · 2020: 40 · 2019: 23 · 2018: 33 · 2017: 37 · 2016: 33 · 2015: 29 · 2014: 40 · 2013: 28 · 2012: 48
FWCI: 1.45
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion)
Open Repository and Bibliography (University of Liège) (submittedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
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 › Visual perception and processing mechanisms
Keywords: hallucinations, auditory hallucinations, visual hallucinations, prefrontal cortex, cingulate cortex, cerebellum, subcortical dysfunction, top-down and bottom-up processes, healthy volunteers
MeSH terms: Brain, Brain Mapping, Hallucinations, Humans, Functional Laterality, Magnetic Resonance Imaging, Positron-Emission Tomography

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The hallucinating brain: A review of structural and functional neuroimaging studies of hallucinations

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