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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“Furthermore, activation in distributed thalamocortical networks has been observed in actively hallucinating patients (Silbersweig et al., 1995).”
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Dysfunction of the Ubiquitin Proteasome and Ubiquitin-Like Systems in Schizophrenia
Rubio, M. D., Wood, K., Haroutunian, V. H., & Meador‐Woodruff, J. H. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.84 · Cited by 138
“The left STG participates in the development of auditory hallucinations (Barta et al, 1990; Nenadic et al, 2010; Silbersweig et al, 1995) and the volume of this cortical area is decreased in subjects with schizophrenia (Sun et al, 2009).”
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“…of schizophrenic patients during auditory and visual hallucinations has shown focal activations in the inner speech and auditory/linguistic association cortices of the brain, providing a biological basis for the subjective reports of schizophrenic patients’ experience (Silbersweig et al, 1995).”
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Ketamine Dose-Dependently Induces High-Frequency Oscillations in the Nucleus Accumbens in Freely Moving Rats
Hunt, M. J., Raynaud, B., & Garcia, R. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.01.020 · Cited by 140
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“Activation in distributed thalamocortical networks has been seen in actively hallucinating patients ( Silbersweig et al. 1995 ).”
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Schizophrenic Patients and Their Unaffected Siblings Share Increased Resting-State Connectivity in the Task-Negative Network but Not Its Anticorrelated Task-Positive Network
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“Specifically, studies attempted to image, in the same person, periods when they were actively hallucinating and when they were not (McGuire et al, 1993; Silbersweig et al, 1995; Shergill et al, 2000; Woodruff et al, 1995).”
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“For example, recent neuroimaging studies of schizophrenics have shown abnormal hippocampal activation during hallucinations (Silbersweig et al 1995).”
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“Indeed, during psychosis, activity within the dorsal striatum was shown to be increased during positive schizophrenia symptoms, including delusions and hallucinations, while during psychotic remission, increased ventral striatal activity was correlated with negative symptoms, including flat affect and emotional withdr…”
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Auditory verbal hallucinations and dysfunction of the neural substrates of speech
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Comparison of the effects of risperidone and haloperidol on regional cerebral blood flow in schizophrenia
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“Neuroimaging studies have revealed that the anterior hippocampus, which is functionally equivalent to the ventral hippocampus in rodents (Grace, 2012), is hyperactive in schizophrenia (Heckers and Konradi, 2015), and the hyperactivity corresponds to psychosis (Silbersweig et al., 1995).”
Background
The hallucinogen 1-[2,5-dimethoxy-4-iodophenyl]-2-aminopropane (DOI) increases cortical extracellular glutamate levels in rats
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“This site of stimulation is believed to overlay Brodmann area 40 (Homan et al., 1987) and was selected in light of results of a previous positron emission tomography (PET) study demonstrating activation in this brain area during AVH (Silbersweig et al., 1995).”
Background
Are Anticorrelated Networks in the Brain Relevant to Schizophrenia?
Williamson, P. (2007) · Schizophrenia Bulletin · doi:10.1093/schbul/sbm043 · Cited by 125
Differences and similarities in the sensory and cognitive signatures of voice-hearing, intrusions and thoughts
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“, 2000), others have failed to find such an increase in activation during AVHs (Lennox et al., 2000; Silbersweig et al., 1995).”
BackgroundMethodResultInfluential
The brain’s voices: comparing nonclinical auditory hallucinations and imagery
Linden, D. E. J., Thornton, K., Kuswanto, C. N., Johnston, S. J., van de Ven, V., & Jackson, M. C. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq097 · Cited by 117
“The activation of fronto temporal and thalamic networks during nonclinical hallucinations coincides with previous reports of brain activity during periods of AVH in schizophrenia patients (Silbersweig et al. 1995; Dierks et al. 1999; Shergill et al. 2000).”
Result
Altered Transcript Expression of NMDA Receptor-Associated Postsynaptic Proteins in the Thalamus of Subjects With Schizophrenia
Clinton, S. M., Haroutunian, V. H., Davis, K. L., & Meador‐Woodruff, J. H. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.6.1100 · Cited by 119
"Where Do Auditory Hallucinations Come From?"--A Brain Morphometry Study of Schizophrenia Patients With Inner or Outer Space Hallucinations
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Tuning in to the Voices: A Multisite fMRI Study of Auditory Hallucinations
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“roimaging study examining such processing in an at-risk population, and the replication of some findings from the schizophrenia literature is noteworthy (Barch, Carter, et al., 2001; Callicott et al., 2000; Epstein et al., 1999; Kircher et al., 2001; Liddle, Friston, Frith, & Frackowiack, 1992; Rubin et al., 1991; Sil…”
Background
A Thalamo-Hippocampal-Ventral Tegmental Area Loop May Produce the Positive Feedback that Underlies the Psychotic Break in Schizophrenia
Lisman, J. E., Pi, H. J., Zhang, Y., & Otmakhova, N. A. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.04.007 · Cited by 123
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Reduced Hippocampal Activation During Encoding and Recognition of Words in Schizophrenia Patients
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Auditory verbal hallucinations as atypical inner speech monitoring, and the potential of neurostimulation as a treatment option
Moseley, P., Fernyhough, C., & Ellison, A. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.10.001 · Cited by 113

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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