Cited by 906Hallucinations in medical conditionsSchizophrenia research and treatmentMental Health and Psychiatry

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A functional neuroanatomy of hallucinations in schizophrenia

Silbersweig, D. A., Stern, E., Frith, C., Cahill, C., Holmes, A., Grootoonk, Sylke, Seaward, J., McKenna, P., Chua, S. E., Schnorr, L., Jones, T., Frackowiak, R. S. J.·1995·Nature

DOI 10.1038/378176a0

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Abstract

Hallucinations, perceptions in the absence of external stimuli, are prominent among the core symptoms of schizophrenia. The neural correlates of these brief, involuntary experiences are not well understood, and have not been imaged selectively. We have used new positron emission tomography (PET) methods to study the brain state associated with the occurrence of hallucinations in six schizophrenic patients. Here we present a group study of five patients with classic auditory verbal hallucinations despite medication, demonstrating activations in subcortical nuclei (thalamic, striatal), limbic structures (especially hippocampus), and paralimbic regions (parahippocampal and cingulate gyri, as well as orbitofrontal cortex). We also present a case study of a unique, drug-naive patient with visual as well as auditory verbal hallucinations, demonstrating activations in visual and auditory/linguistic association cortices as part of a distributed cortical-subcortical network. Activity in deep brain structures, identified with group analysis, may generate or modulate hallucinations, and the particular neocortical regions entrained in individual patients may affect their specific perceptual content. The interaction of these distributed neural systems provides a biological basis for the bizarre reports of schizophrenic patients.

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Background
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Background
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Result
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Background
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“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
Insights and treatment options for psychiatric disorders guided by functional MRI
Sharma, T. (2003) · Journal of Clinical Investigation · doi:10.1172/jci19166 · Cited by 15
“An early study demonstrated activations in subcortical nuclei (thalamic and striatal), limbic structures (especially the hippocampus), and paralimbic regions (parahippocampal and cingulate gyri, as well as orbitofrontal cortex) (41).”
Background
Attention and Schizophrenia: A View from Cognitive Neuroscience
DiGirolamo, G. J. (1996) · Cognitive Neuropsychiatry · doi:10.1080/135468096396578 · Cited by 15
Functional Brain Imaging in Schizophrenia
Meyer‐Lindenberg, A., & Bullmore, E. T. (2010) · Wiley eBooks · doi:10.1002/9781444327298.ch17 · Cited by 16
Map2k7 Haploinsufficiency Induces Brain Imaging Endophenotypes and Behavioral Phenotypes Relevant to Schizophrenia
Openshaw, R. L., Thomson, D. M., Thompson, R., Penninger, J. M., Pratt, J. A., MORRIS, B. J., & Dawson, N. (2019) · Schizophrenia Bulletin · doi:10.1093/schbul/sbz044 · Cited by 15
Lack of Helios During Neural Development Induces Adult Schizophrenia-Like Behaviors Associated With Aberrant Levels of the TRIF-Recruiter Protein WDFY1
Sancho‐Balsells, A., Brito, V., Fernández, B., Pardo, M., Straccia, M., Ginés, S., Alberch, J., Hernández, I., Arranz, B., Canals, J. M., et al. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00093 · Cited by 14
“Interestingly, we and others have shown that, only during development, Helios is also present in neuronal cell subtypes in the striatum and hippocampus (Martín-Ibáñez et al., 2012, 2017), which are key aﬀected brain regions in schizophrenia patients (Silbersweig et al., 1995; Yoon et al., 2013).”
Immune Activation in Pregnant Rats Affects Brain Glucose Consumption, Anxiety-like Behaviour and Recognition Memory in their Male Offspring
Guerrin, C. G. J., Shoji, A., Doorduin, J., & de Vries, E. F. J. (2022) · Molecular Imaging and Biology · doi:10.1007/s11307-022-01723-3 · Cited by 17
“Some clinical studies using [18F]-FDG PET, observed that unmedicated schizophrenia patients displaying positive symptoms had a hypermetabolic status in brain regions, such as the frontal cortex, thalamus, striatum, and temporal lobe [8, 60].”
Background
Auditory hallucinations activate language and verbal short-term memory, but not auditory, brain regions
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
Dynamic neuroimaging with PET, SPET or fMRI
Liddle, P. F. (1997) · International Review of Psychiatry · doi:10.1080/09540269775204 · Cited by 14
Functional and Pharmacological MRI in Understanding Brain Function at a Systems Level
Bifone, A., & Gozzi, A. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_103 · Cited by 14
“This observation is of particular interest given the ample clinical evidence suggesting a correlation between fronto–hippocampal hyperactivity and cognitive and perceptual alterations in unmedicated schizophrenia patients (Parellada et al. 1994; Silbersweig et al. 1995; Liddle et al. 2000; Medoff et al. 2001; Ngan et…”
Background
Les troubles de la reconnaissance de soi : une approche neuropsychologique des symptômes positifs de la schizophrénie
Jeannerod, M. (2003) · médecine/sciences · doi:10.1051/medsci/2003195621 · Cited by 16
“D’autres structures cérébrales, dont les ganglions de la base, sont également impliquées au cours des hallucinations [13].”
Background
Psychopathology Today
Mundt, C., & Spitzer, M. (2001) · Springer eBooks · doi:10.1007/978-3-642-59519-6_1 · Cited by 14
A working model of neural activity and phenomenal experience in psychosis
Martino, M., & Magioncalda, P. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02607-4 · Cited by 14
“On the other hand, the experience of visual hallucinations in schizophrenia is associated with increased activation in the occipito-temporo-parietal cortex (including the cuneus, lingual/ fusiform gyri, and precuneus) mainly involving the secondary/ associative visual areas [66, 69, 76].”
The alternations of nucleus accumbent in schizophrenia patients with auditory verbal hallucinations during low-frequency rTMS treatment
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
“AVH are defined as perceptions in the absence of external verbal stimuli and are prominent among the core symptoms of schizophrenia (32).”
Background
An evolutionary account of impairment of self in cognitive disorders
Benítez‐Burraco, A., Adornetti, I., Ferretti, F., & Progovac, L. (2022) · Cognitive Processing · doi:10.1007/s10339-022-01110-4 · Cited by 14
Thalamic Hyperperfusion in Verbal Hallucination of Parkinsonian Patients
Matsui, H., Nishinaka, K., Miyoshi, T., Hara, N., Oda, M., Kubori, T., & Udaka, F. (2007) · Internal Medicine · doi:10.2169/internalmedicine.46.0191 · Cited by 13
“PET studies also supported increased activity in such regions (28-34).”
Background
Dopamine — Acetylcholine Interactions
Acquas, E., & Chiara, G. D. (2002) · Handbook of experimental pharmacology · doi:10.1007/978-3-662-06765-9_3 · Cited by 14
Unilateral auditory hallucinations in a boy with ipsilateral conductive hearing loss.
Brašić, J. R., & Perry, R. S. (1997) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.62.3.302 · Cited by 13
Functional Neuroimaging—Can It Contribute to Our Understanding of Processes of Change?
Beutel, M. E., & Huber, M. (2008) · Neuropsychoanalysis · doi:10.1080/15294145.2008.10773563 · Cited by 13
“Examples include studies on brain-activity correlates of hallucinations (deep limbic and subcortical as well as neocortical sensory structures: Silbersweig et al., 1995), and Tourette syndrome (aberrant activity in sensorimotor, language, executive, and paralimbic circuits: Stern, Silbersweig, &…”
Background
Regional Alpha-Synuclein Aggregation, Dopaminergic Dysregulation, and the Development of Drug-Related Visual Hallucinations in Parkinson's Disease
Papapetropoulos, S. (2006) · Journal of Neuropsychiatry · doi:10.1176/jnp.2006.18.2.149 · Cited by 13
Symptom Localization in Neuropsychiatry
Silbersweig, D., & Stern, E. R. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48646.x · Cited by 13
Imaging for the clinical psychiatrist: facts, fantasies, and other musings
Brodie, J. D. (1996) · American Journal of Psychiatry · doi:10.1176/ajp.153.2.145 · Cited by 13
On the Neuronal Activity in the Human Brain during Visual Recognition, Imagery and Binocular Rivalry
Kreiman, G. (2002) · CaltechTHESIS (California Institute of Technology) · doi:10.7907/e0xz-qp78 · Cited by 13
What Do Qualia Do?
Gregory, R. L. (1996) · Perception · doi:10.1068/p250377 · Cited by 13
Dysregulated noradrenergic response is associated with symptom severity in individuals with schizophrenia
Pelegrino, A., Guimarães, A. L., Sena, W., Emele, N., Scoriels, L., & Panizzutti, R. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1190329 · Cited by 14
Altered brain morphology and functional connectivity in postmenopausal women: automatic segmentation of whole-brain and thalamic subnuclei and resting-state fMRI
Kim, G.-W., Park, K., Kim, Y., & Jeong, G.-W. (2024) · Aging · doi:10.18632/aging.205662 · Cited by 12
Assessment of treatment resistance criteria in non-invasive brain stimulation studies of schizophrenia
Kronick, J., Sabesan, P., Burhan, A. M., & Palaniyappan, L. K. (2021) · Schizophrenia Research · doi:10.1016/j.schres.2021.06.009 · Cited by 13
The Poly I:C maternal immune stimulation model shows unique patterns of brain metabolism, morphometry, and plasticity in female rats
Casquero‐Veiga, M., Lamanna‐Rama, N., Romero‐Miguel, D., Márquez, H. R., Alcaide, J., Beltrán, M. A. C. S., Nácher, J., Desco, M., & Soto‐Montenegro, M. L. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1022622 · Cited by 12
“In this respect, thalamic hypermetabolism has been associated with psychotic/positive symptoms in schizophrenia and related disorders (Silbersweig et al., 1995; Soyka et al., 2005), and their absence in females may be related to the later onset of these symptoms (Piontkewitz et al.”
Background
Brain mechanisms involved in processing unreal perceptions
Ku, J. H., Kim, J., Jung, Y., Park, I. H., Lee, H., Han, K., Yoon, K. J., Kim, I. Y., & Kim, S. I. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.08.011 · Cited by 12
Mental representation of space: Insights from an oblique distribution of hallucinations
Girard, T. A., Martius, D., & Cheyne, J. A. (2006) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.10.002 · Cited by 12
Clinical, cognitive and neural correlates of self-monitoring deficits in schizophrenia: an update
Raveendran, V., & Kumari, V. (2007) · Acta Neuropsychiatrica · doi:10.1111/j.1601-5215.2007.00151.x · Cited by 13
Resting brain perfusion in alcohol-induced psychotic disorder: A comparison in patients with alcohol dependence, schizophrenia and healthy controls
Jordaan, G. P., Warwick, J., Hewlett, R. H., & Emsley, R. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.01.018 · Cited by 12
“The left parahippocampal gyrus is one of the areas reported to be associated with hallucinations and increased brain activity in patients with schizophrenia (Silbersweig et al., 1995).”
Background
Auditory hallucinations across the psychosis spectrum: Evidence of dysconnectivity involving cerebellar and temporal lobe regions
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
Triangulating perspectives on functional neuroimaging for disorders of mental health
Anderson, J. A., Mizgalewicz, A., & Illes, J. (2013) · BMC Psychiatry · doi:10.1186/1471-244x-13-208 · Cited by 12
Medial septum activation produces opposite effects on dopamine neuron activity in the ventral tegmental area and substantia nigra in MAM vs. normal rats
Bortz, D. M., & Grace, A. A. (2018) · Schizophrenia · doi:10.1038/s41537-018-0059-3 · Cited by 12
Processing of environmental sounds in schizophrenic patients: disordered recognition and lack of semantic specificity
Tüscher, O., Silbersweig, D., Pan, H., Smith, T. E., Beutel, M. E., Zonana, J., Erbesh, V., Weisholtz, D. S., Stern, E. R., & Engelien, A. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2004.06.010 · Cited by 12
“Abnormal temporal lobe activations and interactions have been demonstrated in these regions during this perceptual state (see, e.g. Dierks et al., 1999; Silbersweig et al., 1995).”
Background
Dopamine and Schizophrenia
Abi‐Dargham, A., & Grace, A. A. (2010) · Wiley eBooks · doi:10.1002/9781444327298.ch20 · Cited by 12
Excessive fear of clusters of holes, its interaction with stressful life events and the association with anxiety and depressive symptoms: large epidemiological study of young people in Hong Kong
Wong, S. M. Y., Tang, E. Y. H., Hui, C. L. M., Suen, Y. N., Chan, S. K. W., Lee, E. H. M., Chan, K. T., Wong, M. T. H., Wilkins, A. J., & Chen, E. Y. H. (2023) · BJPsych Open · doi:10.1192/bjo.2023.540 · Cited by 11

Authors: Silbersweig, D. A., Stern, E., Frith, C., Cahill, C., Holmes, A., Grootoonk, S., Seaward, J., McKenna, P., Chua, S. E., Schnorr, L., Jones, T., & Frackowiak, R. S. J.
Affiliations: Hammersmith Hospital (GB)
Fulbourn Hospital (GB)
ORCID: Stern, E.
Frith, C.
Grootoonk, Sylke
McKenna, P.
Jones, T.
Frackowiak, R. S. J.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 1995-11
Volume: 378
Issue: 6553
Pages: 176-179
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/378176a0
OpenAlex: W1969273085
Cited by: 906
References: 30
Citations by year: 2026: 4 · 2025: 8 · 2024: 14 · 2023: 15 · 2022: 20 · 2021: 22 · 2020: 13 · 2019: 18 · 2018: 21 · 2017: 24 · 2016: 27 · 2015: 17 · 2014: 27 · 2013: 25 · 2012: 30
FWCI: 19.72
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
The HKU Scholars Hub (University of Hong Kong) (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: hallucinations, schizophrenia, auditory verbal hallucinations, visual hallucinations, neural correlates, thalamus, striatum, hippocampus, parahippocampal gyrus, cingulate gyrus, orbitofrontal cortex, cortical-subcortical networks
MeSH terms: Adult, Brain, Cerebrovascular Circulation, Hallucinations, Humans, Male, Schizophrenia, Tomography, Emission-Computed

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A functional neuroanatomy of hallucinations in schizophrenia

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