Interaction of language, auditory and memory brain networks in auditory verbal hallucinations

Branislava Ćurčić-Blake, Judith M. Ford, Daniela Hubl, Natasza D. Orlov, Iris E. Sommer, Flavie Waters, Paul Allen, Renaud Jardri, Peter W. Woodruff, Olivier David, Christoph Mulert, Todd S. Woodward, André Aleman

    Research output: Contribution to journalReview article

    51 Citations (Scopus)

    Abstract

    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.

    Original languageEnglish
    Pages (from-to)1-20
    Number of pages20
    JournalProgress in Neurobiology
    Volume148
    DOIs
    Publication statusPublished - 1 Jan 2017

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    Hallucinations
    Language
    Brain
    Corpus Striatum
    Diffusion Tensor Imaging
    Neuroimaging
    Psychotic Disorders
    Electroencephalography
    Magnetic Resonance Imaging

    Cite this

    Ćurčić-Blake, Branislava ; Ford, Judith M. ; Hubl, Daniela ; Orlov, Natasza D. ; Sommer, Iris E. ; Waters, Flavie ; Allen, Paul ; Jardri, Renaud ; Woodruff, Peter W. ; David, Olivier ; Mulert, Christoph ; Woodward, Todd S. ; Aleman, André. / Interaction of language, auditory and memory brain networks in auditory verbal hallucinations. In: Progress in Neurobiology. 2017 ; Vol. 148. pp. 1-20.
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    abstract = "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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    author = "Branislava Ćurčić-Blake and Ford, {Judith M.} and Daniela Hubl and Orlov, {Natasza D.} and Sommer, {Iris E.} and Flavie Waters and Paul Allen and Renaud Jardri and Woodruff, {Peter W.} and Olivier David and Christoph Mulert and Woodward, {Todd S.} and Andr{\'e} Aleman",
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    Ćurčić-Blake, B, Ford, JM, Hubl, D, Orlov, ND, Sommer, IE, Waters, F, Allen, P, Jardri, R, Woodruff, PW, David, O, Mulert, C, Woodward, TS & Aleman, A 2017, 'Interaction of language, auditory and memory brain networks in auditory verbal hallucinations' Progress in Neurobiology, vol. 148, pp. 1-20. https://doi.org/10.1016/j.pneurobio.2016.11.002

    Interaction of language, auditory and memory brain networks in auditory verbal hallucinations. / Ćurčić-Blake, Branislava; Ford, Judith M.; Hubl, Daniela; Orlov, Natasza D.; Sommer, Iris E.; Waters, Flavie; Allen, Paul; Jardri, Renaud; Woodruff, Peter W.; David, Olivier; Mulert, Christoph; Woodward, Todd S.; Aleman, André.

    In: Progress in Neurobiology, Vol. 148, 01.01.2017, p. 1-20.

    Research output: Contribution to journalReview article

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    AU - Ćurčić-Blake, Branislava

    AU - Ford, Judith M.

    AU - Hubl, Daniela

    AU - Orlov, Natasza D.

    AU - Sommer, Iris E.

    AU - Waters, Flavie

    AU - Allen, Paul

    AU - Jardri, Renaud

    AU - Woodruff, Peter W.

    AU - David, Olivier

    AU - Mulert, Christoph

    AU - Woodward, Todd S.

    AU - Aleman, André

    PY - 2017/1/1

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    N2 - 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.

    AB - 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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    KW - Functional connectivity

    KW - Language

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    KW - Psychosis

    KW - Schizophrenia

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