Isn’t it ironic? Neural Correlates of Irony Comprehension in Schizophrenia

Ironic remarks are frequent in everyday language and represent an important form of social cognition. Increasing evidence indicates a deficit in comprehension in schizophrenia. Several models for defective comprehension have been proposed, including possible roles of the medial prefrontal lobe, defa...

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Published inPloS one Vol. 8; no. 9; p. e74224
Main Authors Rapp, Alexander M., Langohr, Karin, Mutschler, Dorothee E., Klingberg, Stefan, Wild, Barbara, Erb, Michael
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 10.09.2013
Public Library of Science (PLoS)
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ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0074224

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Abstract Ironic remarks are frequent in everyday language and represent an important form of social cognition. Increasing evidence indicates a deficit in comprehension in schizophrenia. Several models for defective comprehension have been proposed, including possible roles of the medial prefrontal lobe, default mode network, inferior frontal gyri, mirror neurons, right cerebral hemisphere and a possible mediating role of schizotypal personality traits. We investigated the neural correlates of irony comprehension in schizophrenia by using event-related functional magnetic resonance imaging (fMRI). In a prosody-free reading paradigm, 15 female patients with schizophrenia and 15 healthy female controls silently read ironic and literal text vignettes during fMRI. Each text vignette ended in either an ironic (n = 22) or literal (n = 22) statement. Ironic and literal text vignettes were matched for word frequency, length, grammatical complexity, and syntax. After fMRI, the subjects performed an off-line test to detect error rate. In this test, the subjects indicated by button press whether the target sentence has ironic, literal, or meaningless content. Schizotypal personality traits were assessed using the German version of the schizotypal personality questionnaire (SPQ). Patients with schizophrenia made significantly more errors than did the controls (correct answers, 85.3% vs. 96.3%) on a behavioural level. Patients showed attenuated blood oxygen level-dependent (BOLD) response during irony comprehension mainly in right hemisphere temporal regions (ironic>literal contrast) and in posterior medial prefrontal and left anterior insula regions (for ironic>visual baseline, but not for literal>visual baseline). In patients with schizophrenia, the parahippocampal gyrus showed increased activation. Across all subjects, BOLD response in the medial prefrontal area was negatively correlated with the SPQ score. These results highlight the role of the posterior medial prefrontal and right temporal regions in defective irony comprehension in schizophrenia and the mediating role of schizotypal personality traits.
AbstractList Ironic remarks are frequent in everyday language and represent an important form of social cognition. Increasing evidence indicates a deficit in comprehension in schizophrenia. Several models for defective comprehension have been proposed, including possible roles of the medial prefrontal lobe, default mode network, inferior frontal gyri, mirror neurons, right cerebral hemisphere and a possible mediating role of schizotypal personality traits. We investigated the neural correlates of irony comprehension in schizophrenia by using event-related functional magnetic resonance imaging (fMRI). In a prosody-free reading paradigm, 15 female patients with schizophrenia and 15 healthy female controls silently read ironic and literal text vignettes during fMRI. Each text vignette ended in either an ironic (n = 22) or literal (n = 22) statement. Ironic and literal text vignettes were matched for word frequency, length, grammatical complexity, and syntax. After fMRI, the subjects performed an off-line test to detect error rate. In this test, the subjects indicated by button press whether the target sentence has ironic, literal, or meaningless content. Schizotypal personality traits were assessed using the German version of the schizotypal personality questionnaire (SPQ). Patients with schizophrenia made significantly more errors than did the controls (correct answers, 85.3% vs. 96.3%) on a behavioural level. Patients showed attenuated blood oxygen level-dependent (BOLD) response during irony comprehension mainly in right hemisphere temporal regions (ironic>literal contrast) and in posterior medial prefrontal and left anterior insula regions (for ironic>visual baseline, but not for literal>visual baseline). In patients with schizophrenia, the parahippocampal gyrus showed increased activation. Across all subjects, BOLD response in the medial prefrontal area was negatively correlated with the SPQ score. These results highlight the role of the posterior medial prefrontal and right temporal regions in defective irony comprehension in schizophrenia and the mediating role of schizotypal personality traits.
Ironic remarks are frequent in everyday language and represent an important form of social cognition. Increasing evidence indicates a deficit in comprehension in schizophrenia. Several models for defective comprehension have been proposed, including possible roles of the medial prefrontal lobe, default mode network, inferior frontal gyri, mirror neurons, right cerebral hemisphere and a possible mediating role of schizotypal personality traits. We investigated the neural correlates of irony comprehension in schizophrenia by using event-related functional magnetic resonance imaging (fMRI). In a prosody-free reading paradigm, 15 female patients with schizophrenia and 15 healthy female controls silently read ironic and literal text vignettes during fMRI. Each text vignette ended in either an ironic (n = 22) or literal (n = 22) statement. Ironic and literal text vignettes were matched for word frequency, length, grammatical complexity, and syntax. After fMRI, the subjects performed an off-line test to detect error rate. In this test, the subjects indicated by button press whether the target sentence has ironic, literal, or meaningless content. Schizotypal personality traits were assessed using the German version of the schizotypal personality questionnaire (SPQ). Patients with schizophrenia made significantly more errors than did the controls (correct answers, 85.3% vs. 96.3%) on a behavioural level. Patients showed attenuated blood oxygen level-dependent (BOLD) response during irony comprehension mainly in right hemisphere temporal regions (ironic>literal contrast) and in posterior medial prefrontal and left anterior insula regions (for ironic>visual baseline, but not for literal>visual baseline). In patients with schizophrenia, the parahippocampal gyrus showed increased activation. Across all subjects, BOLD response in the medial prefrontal area was negatively correlated with the SPQ score. These results highlight the role of the posterior medial prefrontal and right temporal regions in defective irony comprehension in schizophrenia and the mediating role of schizotypal personality traits.Ironic remarks are frequent in everyday language and represent an important form of social cognition. Increasing evidence indicates a deficit in comprehension in schizophrenia. Several models for defective comprehension have been proposed, including possible roles of the medial prefrontal lobe, default mode network, inferior frontal gyri, mirror neurons, right cerebral hemisphere and a possible mediating role of schizotypal personality traits. We investigated the neural correlates of irony comprehension in schizophrenia by using event-related functional magnetic resonance imaging (fMRI). In a prosody-free reading paradigm, 15 female patients with schizophrenia and 15 healthy female controls silently read ironic and literal text vignettes during fMRI. Each text vignette ended in either an ironic (n = 22) or literal (n = 22) statement. Ironic and literal text vignettes were matched for word frequency, length, grammatical complexity, and syntax. After fMRI, the subjects performed an off-line test to detect error rate. In this test, the subjects indicated by button press whether the target sentence has ironic, literal, or meaningless content. Schizotypal personality traits were assessed using the German version of the schizotypal personality questionnaire (SPQ). Patients with schizophrenia made significantly more errors than did the controls (correct answers, 85.3% vs. 96.3%) on a behavioural level. Patients showed attenuated blood oxygen level-dependent (BOLD) response during irony comprehension mainly in right hemisphere temporal regions (ironic>literal contrast) and in posterior medial prefrontal and left anterior insula regions (for ironic>visual baseline, but not for literal>visual baseline). In patients with schizophrenia, the parahippocampal gyrus showed increased activation. Across all subjects, BOLD response in the medial prefrontal area was negatively correlated with the SPQ score. These results highlight the role of the posterior medial prefrontal and right temporal regions in defective irony comprehension in schizophrenia and the mediating role of schizotypal personality traits.
Audience Academic
Author Erb, Michael
Klingberg, Stefan
Rapp, Alexander M.
Mutschler, Dorothee E.
Wild, Barbara
Langohr, Karin
AuthorAffiliation 2 Department of Neurology, Marienhospital Stuttgart, Stuttgart, Germany
1 Department of Psychiatry, University of Tuebingen, Tuebingen, Germany
Hangzhou Normal University, China
3 Biomedical Magnetic Resonance, Department of Radiology, University of Tuebingen, Tuebingen, Germany
AuthorAffiliation_xml – name: 2 Department of Neurology, Marienhospital Stuttgart, Stuttgart, Germany
– name: Hangzhou Normal University, China
– name: 1 Department of Psychiatry, University of Tuebingen, Tuebingen, Germany
– name: 3 Biomedical Magnetic Resonance, Department of Radiology, University of Tuebingen, Tuebingen, Germany
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  givenname: Alexander M.
  surname: Rapp
  fullname: Rapp, Alexander M.
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  givenname: Karin
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  givenname: Dorothee E.
  surname: Mutschler
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  givenname: Stefan
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  fullname: Erb, Michael
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24040207$$D View this record in MEDLINE/PubMed
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2013 Rapp et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2013 Rapp et al 2013 Rapp et al
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Conceived and designed the experiments: AMR KL DEM BW ME. Performed the experiments: AMR KL DEM ME. Analyzed the data: AMR KL DEM ME. Contributed reagents/materials/analysis tools: ME. Wrote the paper: AMR KL DEM SK BW ME.
Competing Interests: The authors have declared that no competing interests exist.
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SubjectTerms Adult
Brain
Brain Mapping
Case-Control Studies
Cognition
Comprehension
Defects
Error detection
Evoked Potentials, Auditory
Female
Functional Laterality
Functional magnetic resonance imaging
Hallucinations
Hemispheric laterality
Humans
Language
Linguistics
Magnetic resonance
Magnetic Resonance Imaging
Mental disorders
Neurons
Neurophysiology
Neurosciences
Oxygen
Parahippocampal gyrus
Parahippocampal Gyrus - pathology
Parahippocampal Gyrus - physiopathology
Patients
Personal communication
Personality
Prefrontal Cortex - pathology
Prefrontal Cortex - physiopathology
Psychiatry
Psychological Tests
Psychopathology
Schizophrenia
Schizophrenia - physiopathology
Schizophrenic Psychology
Social interactions
Surveys and Questionnaires
Theory
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Title Isn’t it ironic? Neural Correlates of Irony Comprehension in Schizophrenia
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http://dx.doi.org/10.1371/journal.pone.0074224
Volume 8
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