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Aberrant attentive and inattentive brain activity to auditory negative words, and its relation to persecutory delusion in patients with schizophrenia

Authors Iwashiro N, Takano Y, Natsubori T, Aoki Y, Yahata N, Gonoi W, Kunimatsu A, Abe O, Kasai K, Yamasue H

Received 13 November 2018

Accepted for publication 11 January 2019

Published 14 February 2019 Volume 2019:15 Pages 491—502


Checked for plagiarism Yes

Review by Single anonymous peer review

Peer reviewer comments 2

Editor who approved publication: Dr Taro Kishi

Norichika Iwashiro,1 Yosuke Takano,1 Tatsunobu Natsubori,1 Yuta Aoki,1 Noriaki Yahata,1,2 Wataru Gonoi,3 Akira Kunimatsu,3 Osamu Abe,3 Kiyoto Kasai,1 Hidenori Yamasue4

1Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo, Japan; 2Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, Chiba-city, Chiba, Japan; 3Department of Radiology, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Japan; 4Department of Psychiatry, Hamamatsu University School of Medicine, Higashi-ku, Hamamatsu City, Japan

Background and purpose: Previous research has suggested that deficits in emotion recognition are involved in the pathogenesis of persecutory delusion in schizophrenia. Although disruption in auditory and language processing is crucial in the pathophysiology of schizophrenia, the neural basis for the deficits in emotion recognition of auditorily presented language stimuli and its relation to persecutory delusion have not yet been clarified.
Patients and methods: The current functional magnetic resonance imaging study used a dichotic listening task for 15 patients with schizophrenia and 23 healthy controls matched for age, sex, parental socioeconomic background, handedness, dexterous ear, and intelligence quotient. The participants completed a word recognition task on the attended side in which a word with emotionally valenced content (negative/neutral) was presented to one ear and a different neutral word was presented to the other ear. Participants selectively attended to either ear.
Results: The whole brain analysis detected the aberrant neural activity in the right inferior frontal gyrus in the patients with schizophrenia compared to that in the controls (P<0.05, false discovery rate-corrected). Brain activity in the right pars triangularis of the inferior frontal gyrus was significantly reduced when negatively valenced words were presented to the right ear, whereas the activity of the same region was significantly enhanced when these words were presented to the left ear, irrespective of the attended ear, in the participants with schizophrenia compared to the controls. Furthermore, this diminished brain response to auditorily presented negatively valenced words significantly correlated with severe positive symptoms (r=-0.67, P=0.006) and delusional behavior (r=-0.62, P=0.014) in the patients with schizophrenia.
Conclusion: The present results indicate that the significantly impaired brain activity in response to auditorily presented negatively valenced words in the right pars triangularis of the inferior frontal gyrus is associated with the pathogenesis of positive symptoms such as persecutory delusion.

Keywords: auditory perception, inferior frontal gyrus, emotion, language, functional magnetic resonance imaging, psychosis

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