Differential responses from the left postcentral gyrus, right middle frontal gyrus, and precuneus to meal ingestion in patients with functional dyspepsia

Yiping Chen; Risheng Yu; Joseph F X DeSouza; Yuze Shen; Hanyun Zhang; Chunpeng Zhu; Peiyu Huang; Caihua Wang

doi:10.3389/fpsyt.2023.1184797

Differential responses from the left postcentral gyrus, right middle frontal gyrus, and precuneus to meal ingestion in patients with functional dyspepsia

Front Psychiatry. 2023 May 19:14:1184797. doi: 10.3389/fpsyt.2023.1184797. eCollection 2023.

Authors

Yiping Chen¹, Risheng Yu², Joseph F X DeSouza^{3

4}, Yuze Shen⁵, Hanyun Zhang⁶, Chunpeng Zhu⁶, Peiyu Huang², Caihua Wang⁶

Affiliations

¹ Department of Psychiatry, Zhejiang University School of Medicine Second Affiliated Hospital, Hangzhou, Zhejiang, China.
² Department of Radiology, Zhejiang University School of Medicine Second Affiliated Hospital, Hangzhou, Zhejiang, China.
³ Department of Psychology and Biology, Neuroscience Graduate Diploma Program and Graduate Program in Interdisciplinary Studies, Multisensory Neuroscience Laboratory, Centre for Vision Research, York University, Toronto, ON, Canada.
⁴ VISTA and Canadian Action and Perception Network (CAPnet), Toronto, ON, Canada.
⁵ Department of Psychiatry, First People's Hospital, Hangzhou, China.
⁶ Department of Gastroenterology, Zhejiang University School of Medicine Second Affiliated Hospital, Hangzhou, China.

Abstract

Background: Functional dyspepsia (FD) is most often a meal-induced syndrome. Studies using resting-state functional magnetic resonance imaging (rs-fMRI) reported abnormal connectivity in areas related to pain processing in FD. However, only a few studies have attempted to determine how meal ingestion affects the brain's working patterns. Through rs-fMRI, this study observed how meal ingestion affected brain regions related to visceral hypersensitivity and emotional response networks in FD patients.

Methods: A total of 30 FD patients and 32 healthy controls (HC) were enrolled and underwent clinical investigations. Rs-fMRI was performed twice after a 4-h fast and 50 min after a meal. The mean functional connectivity strength (FCS) values were extracted from brain regions with significant differences to show the trend of changes related to meal ingestion after FCS analyses.

Results: Depression, anxiety, sleep disturbances, and weight loss were more common in FD patients (P ≤ 0.001). Compared with HCs (corrected cluster P-value < 0.05), FD patients had significantly higher FCS in the right middle frontal gyrus before meals and higher meal-induced FCS in the left postcentral gyrus. HCs had greater meal-induced activation in the right precuneus and anterior cingulate cortex. FD patients had a decreasing trend in the right inferior frontal gyrus compared to the increasing trend in HCs. We only found anxiety to be negatively correlated with FCS in the right inferior frontal gyrus in FD (r = -0.459, p = 0.048, uncorrected).

Conclusions: In this study, we discovered that FD patients have different perceptual and emotional responses to food intake in defined brain areas, providing promising impetus for understanding pathogenic brain mechanisms in FD.

Keywords: anterior cingulate cortex; functional connectivity; functional dyspepsia; left postcentral gyrus; meal ingestion; right inferior frontal gyrus; right middle frontal gyrus; right precuneus.