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

• Published in: NeuroImage clinical Vol. 15; pp. 525 - 540
• Main Authors: Adamczyk, Przemysław, Wyczesany, Miroslaw, Domagalik, Aleksandra, Daren, Artur, Cepuch, Kamil, Błądziński, Piotr, Cechnicki, Andrzej, Marek, Tadeusz
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier Inc 01.01.2017; Elsevier
• Subjects: Adult; Brain - diagnostic imaging; Brain - physiopathology; Communication skills; Comprehension - physiology; Female; Figurative meaning; Functional magnetic resonance imaging; Humans; Humor; Magnetic Resonance Imaging - methods; Male; Middle Aged; Nerve Net - diagnostic imaging; Nerve Net - physiopathology; Radiology; Regular; Schizophrenia; Schizophrenia - diagnostic imaging; Schizophrenia - physiopathology; Schizophrenic Psychology; Verbal Learning - physiology; Wit and Humor as Topic - psychology; MTG; IPL; MoCA; STG; GLM; RHLB; sLORETA; PFC; ToM; dmMFG; Functional magnetic resonance imaging; PANSS; pSTG; EEG; ERPs; fMRI; Communication skills; dlPFC; FWHM; SEM; BA; RT; MRI; ns; Schizophrenia; MNI; IFG; L; MFG; TPJ; SD; ABS; R; dACC; FDR; SFG; FUN; ISI; ACC; CON; fNIRS; MOG; SOA; Figurative meaning; k; Humor; SCH; TP; NEU; non-significant group difference; Montreal Cognitive Assessment; left hemisphere; dorsolateral prefrontal cortex; healthy controls/control group; EEG event-related potentials; standard deviations; Inferior Parietal Lobule; anterior cingulate cortex; middle temporal gyrus; temporal pole; schizophrenia outpatients/clinical group; absurd/nonsensical punchline; inferior frontal gyrus; full-width-at-half-maximum; general linear model; functional near-infrared spectroscopy; reaction time; standard error of the mean; superior temporal gyrus; magnetic resonance imaging; theory of mind; prefrontal cortex; posterior Superior Temporal Gyrus; stimulus onset asynchrony; Right Hemisphere Language Battery; Positive and Negative Syndrome Scale; number of voxels in analyzed cluster size; dorsal anterior cingulate cortex; right hemisphere; interstimulus-interval; funny punchline; standardized low resolution brain electromagnetic tomography analysis; Montreal Neurological Institute coordinates; False Discovery Rate; dorsomedial Middle Frontal Gyrus; electroencephalography; neutral/unfunny punchline; middle occipital gyrus; Brodmann's area; medial frontal gyrus; Superior Frontal Gyrus; temporoparietal junction; ToM, theory of mind; FWHM, full-width-at-half-maximum; L, left hemisphere; FUN, funny punchline; pSTG, posterior Superior Temporal Gyrus; IFG, inferior frontal gyrus; PANSS, Positive and Negative Syndrome Scale; ERPs, EEG event-related potentials; TPJ, temporoparietal junction; MoCA, Montreal Cognitive Assessment; fMRI, functional magnetic resonance imaging; IPL, Inferior Parietal Lobule; dmMFG, dorsomedial Middle Frontal Gyrus; R, right hemisphere; sLORETA, standardized low resolution brain electromagnetic tomography analysis; TP, temporal pole; EEG, electroencephalography; dlPFC, dorsolateral prefrontal cortex; ACC, anterior cingulate cortex; MOG, middle occipital gyrus; PFC, prefrontal cortex; STG, superior temporal gyrus; GLM, general linear model; SFG, Superior Frontal Gyrus; fNIRS, functional near-infrared spectroscopy; RHLB, Right Hemisphere Language Battery; SD, standard deviations; ABS, absurd/nonsensical punchline; k, number of voxels in analyzed cluster size; MFG, medial frontal gyrus; dACC, dorsal anterior cingulate cortex; FDR, False Discovery Rate; NEU, neutral/unfunny punchline; SEM, standard error of the mean; MNI, Montreal Neurological Institute coordinates; CON, healthy controls/control group; MTG, middle temporal gyrus; MRI, magnetic resonance imaging; SOA, stimulus onset asynchrony; ISI, interstimulus-interval; BA, Brodmann's area; ns, non-significant group difference; RT, reaction time; SCH, schizophrenia outpatients/clinical group
• ISSN: 2213-1582; 2213-1582
• DOI: 10.1016/j.nicl.2017.06.005

Individuals with schizophrenia exhibit problems with understanding the figurative meaning of language. This study evaluates neural correlates of diminished humor comprehension observed in schizophrenia. The study included chronic schizophrenia (SCH) outpatients (n=20), and sex, age and education level matched healthy controls (n=20). The fMRI punchline based humor comprehension task consisted of 60 stories of which 20 had funny, 20 nonsensical and 20 neutral (not funny) punchlines. After the punchlines were presented, the participants were asked to indicate whether the story was comprehensible and how funny it was. Three contrasts were analyzed in both groups reflecting stages of humor processing: abstract vs neutral stories - incongruity detection; funny vs abstract - incongruity resolution and elaboration; and funny vs neutral – complete humor processing. Additionally, parametric modulation analysis was performed using both subjective ratings separately. Between-group comparisons revealed that the SCH subjects had attenuated activation in the right posterior superior temporal gyrus (BA 41) in case of irresolvable incongruity processing of nonsensical puns; in the left dorsomedial middle and superior frontal gyri (BA 8/9) in case of incongruity resolution and elaboration processing of funny puns; and in the interhemispheric dorsal anterior cingulate cortex (BA 24) in case of complete processing of funny puns. Additionally, during comprehensibility ratings the SCH group showed a suppressed activity in the left dorsomedial middle and superior frontal gyri (BA 8/9) and revealed weaker activation during funniness ratings in the left dorsal anterior cingulate cortex (BA 24). Interestingly, these differences in the SCH group were accompanied behaviorally by a protraction of time in both types of rating responses and by indicating funny punchlines less comprehensible. Summarizing, our results indicate neural substrates of humor comprehension processing impairments in schizophrenia, which is accompanied by fronto-temporal hypoactivation. •Schizophrenia outpatients revealed impairments in humor comprehension processing.•Neural processing was impaired at three stages of the humor comprehension process.•Incongruity detection - hypofunction in the right temporal lobe in schizophrenia.•Resolution & Elaboration - hypofunction in the left frontal lobe in schizophrenia.•Complete process - hypofunction in the anterior cingulate cortex in schizophrenia.