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 in | PloS one Vol. 8; no. 9; p. e74224 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
10.09.2013
Public Library of Science (PLoS) |
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Online Access | Get full text |
ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/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. |
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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 |
Author_xml | – sequence: 1 givenname: Alexander M. surname: Rapp fullname: Rapp, Alexander M. – sequence: 2 givenname: Karin surname: Langohr fullname: Langohr, Karin – sequence: 3 givenname: Dorothee E. surname: Mutschler fullname: Mutschler, Dorothee E. – sequence: 4 givenname: Stefan surname: Klingberg fullname: Klingberg, Stefan – sequence: 5 givenname: Barbara surname: Wild fullname: Wild, Barbara – sequence: 6 givenname: Michael surname: Erb fullname: Erb, Michael |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24040207$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2013 Public Library of Science 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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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 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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Snippet | Ironic remarks are frequent in everyday language and represent an important form of social cognition. Increasing evidence indicates a deficit in comprehension... |
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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 |
URI | https://www.ncbi.nlm.nih.gov/pubmed/24040207 https://www.proquest.com/docview/1431404932 https://www.proquest.com/docview/1433266659 https://pubmed.ncbi.nlm.nih.gov/PMC3769349 https://doaj.org/article/80043438b8b54f37b22d7bed65fc07af http://dx.doi.org/10.1371/journal.pone.0074224 |
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