Neural circuit of verbal humor comprehension in schizophrenia - an fMRI study

Adamczyk, Przemysław; Wyczesany, Mirosław; Domagalik, Aleksandra; Daren, Artur; Cepuch, Kamil; Błądziński, Piotr; Cechnicki, Andrzej; Marek, Tadeusz

doi:10.1016/j.nicl.2017.06.005

Cited by 28 publications

(34 citation statements)

References 106 publications

(237 reference statements)

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“…We found that the difficulties with comprehension of figurative meaning were related either to the (i) general problems with language comprehension, (ii) problems with understanding of figurative meaning within context, but with proper recognition of conventional metaphors, or iii) with more often figurative misinterpretation of literal meaning. Regarding neural substrates of the observed impairment, the fMRI data revealed that the diminished ability to comprehend conventional metaphors observed in schizophrenia is related to the bilateral, but dominantly leftward-shifted fronto-temporo-parietal brain regions First of all, the frontal hypofunction of the interhemispheric dorsal ACC and left MFG/SFG is consistent with previous data on diminished humor comprehension as another impaired figurative aspect of language in schizophrenia (Adamczyk et al 2017;Berger et al 2018;Vrticka et al 2013). This could reflect the cognitive deficiencies, e.g.…”

Section: Discussionsupporting

confidence: 89%

“…Finally, effective connectivity maps were created to reveal the between-group differences in the information flow between specified ROIs of figurative language-related networks. Data were visualized using Trand3D 1.2 software (Department of Biomedical Physics, University of Warsaw; Blinowski et al 2014) in three pairs of directional contrasts, based on previously assessed contrasts from humor experiments (Adamczyk et al 2017(Adamczyk et al , 2019Chan et al 2012Chan et al , 2013: ABS vs NEU, MET vs ABS, MET vs NEU. Effective connectivity maps were created to reveal the between-group differences in the information flow.…”

Section: Discussionmentioning

confidence: 99%

“…answers) consisting of metaphorical sentences; they were then adapted to create three types of endings, i.e. NEU, ABS, MET following the punchline-based humor comprehension task procedure (Adamczyk et al 2017(Adamczyk et al , 2019. Next, 612 stories were divided into three separate sets (3 × 68 MET, 68 NEU, 68 ABS), thus ensuring that each person rated only one version of the same story/setup; they were then presented for pre-selective judgment to 60 healthy people (25 males, 35 females; mean age 27.65 ± 6.44 SD, min.…”

Section: Punchline-based Metaphor Comprehension Taskmentioning

confidence: 99%

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On the Role of Bilateral Brain Hypofunction and Abnormal Lateralization of Cortical Information Flow as Neural Underpinnings of Conventional Metaphor Processing Impairment in Schizophrenia: An fMRI and EEG Study

et al. 2021

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Figurative language processing (e.g. metaphors) is commonly impaired in schizophrenia. In the present study, we investigated the neural activity and propagation of information within neural circuits related to the figurative speech, as a neural substrate of impaired conventional metaphor processing in schizophrenia. The study included 30 schizophrenia outpatients and 30 healthy controls, all of whom were assessed with a functional Magnetic Resonance Imaging (fMRI) and electroencephalography (EEG) punchline-based metaphor comprehension task including literal (neutral), figurative (metaphorical) and nonsense (absurd) endings. The blood oxygenation level-dependent signal was recorded with 3T MRI scanner and direction and strength of cortical information flow in the time course of task processing was estimated with a 64-channel EEG input for directed transfer function. The presented results revealed that the behavioral manifestation of impaired figurative language in schizophrenia is related to the hypofunction in the bilateral fronto-temporo-parietal brain regions (fMRI) and various differences in effective connectivity in the fronto-temporo-parietal circuit (EEG). Schizophrenia outpatients showed an abnormal pattern of connectivity during metaphor processing which was related to bilateral (but more pronounced at the left hemisphere) hypoactivation of the brain. Moreover, we found reversed lateralization patterns, i.e. a rightward-shifted pattern during metaphor processing in schizophrenia compared to the control group. In conclusion, the presented findings revealed that the impairment of the conventional metaphor processing in schizophrenia is related to the bilateral brain hypofunction, which supports the evidence on reversed lateralization of the language neural network and the existence of compensatory recruitment of alternative neural circuits in schizophrenia.

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Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: Punchline-based Metaphor Comprehension Taskmentioning

confidence: 99%

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On the Role of Bilateral Brain Hypofunction and Abnormal Lateralization of Cortical Information Flow as Neural Underpinnings of Conventional Metaphor Processing Impairment in Schizophrenia: An fMRI and EEG Study

et al. 2021

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“…Although the schizophrenia group exhibited a similar level of subjective amusement behaviorally, they may not have understood the humor in the same manner as the controls. An fMRI study using relatively short sentences and punchlines 22 discovered that patients with schizophrenia had attenuated BOLD signals in several frontal areas—including the left dorsomedial middle and superior frontal gyri (BA 8/9) and the interhemispheric dorsal anterior cingulate cortex (BA 24)—during the various stages of humor processing. Given the previous theory about the cognitive and emotional components of humor, our findings of lower ISC in the fronto-parietal areas support that schizophrenia patients have the deficit of cognitive processing of humor because of the anatomical overlap.…”

Section: Discussionmentioning

confidence: 99%

Reduced synchronized brain activity in schizophrenia during viewing of comedy movies

Lin

et al. 2019

Sci Rep

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Previous evaluation of brain function in schizophrenia has focused on standard experimental tasks, with cerebral response to natural stimuli less clear. This study employed inter-subject correlation (ISC) analysis to investigate the neural basis of humor processing during free viewing of comedy movies in patients with schizophrenia. We recruited 29 patients diagnosed with schizophrenia and 29 healthy, age- and sex-matched controls. Each participant underwent fMRI scanning during two viewings of three comedy movie clips. The ISC map from each participant pair within each population group and each movie viewing was separately derived. The significance of ISC within a group and between two groups were assessed by bootstrapping. The ISC map from each patient pair were also correlated with the product of Positive and Negative Syndrome Scale (PANSS) rating between the same participant pair in schizophrenia patients. Schizophrenia patients showed significant ISC in bilateral lateraloccipital, bilateral superior frontal, left supramarginal, and right lateralorbiofrontal cortices. Compared with the controls, the schizophrenia group exhibited significantly lower ISC in the left superior temporal sulcus, bilateral supramarginal, and bilateral inferiorparietal cortices. Higher clinical severity (higher total PANSS rating) was associated with lower ISC in the middle frontal and middle temporal regions, and also higher ISC in the visual cortex, inferior temporal gyrus, and anterior cingulate. The findings indicated that patients with schizophrenia are characterized by lower ISC in a frontal parietal network while viewing comedy film clips, which implicated a deficit in the cognitive component of humor processing. The lower synchronization in parts of the frontal parietal network also correlated with symptom severity.

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“…Neural activity in the regions that comprise substantial elements of the DMN has been demonstrated to occur during a process of self-oriented mentation in numerous studies ( Baars, 2010 , Gruberger et al, 2011 , Stawarczyk et al, 2011 ). In addition, involvement of mental imagery in schizophrenia as a source of increased activation in the precuneus has been discussed in previous fMRI studies, which investigated cartoon jokes in individuals with enhanced risk of schizophrenia ( Marjoram et al, 2006 ), comprehension of the figurative meaning of language, such as metaphor ( Mashal et al, 2014 ) or verbal humor ( Adamczyk et al, 2017 ) in patients with schizophrenia. Moreover, hyper-activation in the DMN has been shown in patients with schizophrenia during task-related functioning suggesting inability to suppress non-relevant thinking ( Bleich-Cohen et al, 2012 ).…”

Section: Discussionmentioning

confidence: 99%

Abnormal neural hierarchy in processing of verbal information in patients with schizophrenia

Lerner

Bleich-Cohen

Solnik-Knirsh

et al. 2018

NeuroImage: Clinical

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Previous research indicates abnormal comprehension of verbal information in patients with schizophrenia. Yet the neural mechanism underlying the breakdown of verbal information processing in schizophrenia is poorly understood. Imaging studies in healthy populations have shown a network of brain areas involved in hierarchical processing of verbal information over time. Here, we identified critical aspects of this hierarchy, examining patients with schizophrenia. Using functional magnetic resonance imaging, we examined various levels of information comprehension elicited by naturally presented verbal stimuli; from a set of randomly shuffled words to an intact story. Specifically, patients with first episode schizophrenia (N = 15), their non-manifesting siblings (N = 14) and healthy controls (N = 15) listened to a narrated story and randomly scrambled versions of it. To quantify the degree of dissimilarity between the groups, we adopted an inter-subject correlation (inter-SC) approach, which estimates differences in synchronization of neural responses within and between groups. The temporal topography found in healthy and siblings groups were consistent with our previous findings – high synchronization in responses from early sensory toward high order perceptual and cognitive areas. In patients with schizophrenia, stimuli with short and intermediate temporal scales evoked a typical pattern of reliable responses, whereas story condition (long temporal scale) revealed robust and widespread disruption of the inter-SCs. In addition, the more similar the neural activity of patients with schizophrenia was to the average response in the healthy group, the less severe the positive symptoms of the patients. Our findings suggest that system-level neural indication of abnormal verbal information processing in schizophrenia reflects disease manifestations.

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Neural circuit of verbal humor comprehension in schizophrenia - an fMRI study

Cited by 28 publications

References 106 publications

On the Role of Bilateral Brain Hypofunction and Abnormal Lateralization of Cortical Information Flow as Neural Underpinnings of Conventional Metaphor Processing Impairment in Schizophrenia: An fMRI and EEG Study

On the Role of Bilateral Brain Hypofunction and Abnormal Lateralization of Cortical Information Flow as Neural Underpinnings of Conventional Metaphor Processing Impairment in Schizophrenia: An fMRI and EEG Study

Reduced synchronized brain activity in schizophrenia during viewing of comedy movies

Abnormal neural hierarchy in processing of verbal information in patients with schizophrenia

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