Abstract
Functional magnetic resonance imaging (fMRI), electroencephalogram (EEG), and diffusion tensor imaging (DTI) recording have complementary spatiotemporal resolution limitations but can be powerful methods when used together to enable both functional and anatomical modeling, with each neuroimaging procedure used to maximum advantage. We recorded EEGs during event-related fMRI followed by DTI in 15 healthy volunteers and 12 patients with schizophrenia using an omission mismatch negativity (MMN) paradigm. Blood oxygenation level-dependent (BOLD) signal changes were calculated in a region of interest (ROI) analysis, and fractional anisotropy (FA) in the white matter fibers related to each area was compared between groups using tract-specific analysis. Patients with schizophrenia had reduced BOLD activity in the left middle temporal gyrus, and BOLD activity in the right insula and right parahippocampal gyrus significantly correlated with positive symptoms on the Positive and Negative Syndrome Scale (PANSS) and hostility subscores. BOLD activation of Heschl’s gyri also correlated with the limbic system, including the insula. FA values in the left anterior cingulate cortex (ACC) significantly correlated with changes in the BOLD signal in the right superior temporal gyrus (STG), and FA values in the right ACC significantly correlated with PANSS scores. This is the first study to examine MMN using simultaneous fMRI, EEG, and DTI recording in patients with schizophrenia to investigate the potential implications of abnormalities in the ACC and limbic system, including the insula and parahippocampal gyrus, as well as the STG. Structural changes in the ACC during schizophrenia may represent part of the neural basis for the observed MMN deficits. The deficits seen in the feedback/feedforward connections between the prefrontal cortex and STG modulated by the ACC and insula may specifically contribute to impaired MMN generation and clinical manifestations.
Highlights
We examined the correlation between Diffusion tensor imaging (DTI), mismatch negativity (MMN), and Functional magnetic resonance imaging (fMRI) to clarify the association between the phenotypes reflected by fMRI and EEG
The significant correlation between Blood oxygenation level-dependent (BOLD) activity in the right superior temporal gyrus (STG) and MMN amplitudes suggests that the phenomenon seen on fMRI may be a counterpart to the MMN component recorded on the EEG
Causal inferences should be considered with caution given the limitations, the deficits of the feedback/feed-forward connection between the prefrontal cortex and STG modulated by the anterior cingulate cortex (ACC) and insula may contribute to impaired MMN generation and clinical manifestations in schizophrenia
Summary
Ethical statementThis study was approved by the Juntendo University Koshigaya Hospital Ethics Committee and Juntendo University Shizuoka Hospital Ethics Committee. Attempts were made to match the groups for years of education, but this proved to be difficult because patients with schizophrenia are more likely to require hospitalization and the early age of onset [32], which can interfere with schooling. Patients were recruited from among the outpatients at Juntendo University Koshigaya Hospital in Saitama and Juntendo University Shizuoka Hospital in Shizuoka, Japan, and healthy controls were recruited from the staff of the same hospitals. The DSM-5 [33] diagnosis and Positive and Negative Syndrome Scale (PANSS) [34] score were determined for each patient using a structured psychiatric interview and by reviewing the patients’ medical charts. The mean PANSS scores were 15.4±6.9 (positive scales), 22.8±9.2
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