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      Abnormal Functional Connectivity Between the Left Medial Superior Frontal Gyrus and Amygdala Underlying Abnormal Emotion and Premature Ejaculation: A Resting State fMRI Study

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          Abstract

          Introduction

          Premature ejaculation (PE) is a common sexual dysfunction and is found to be associated with abnormal emotion. The amygdala plays an important role in the processing of emotion. The process of ejaculation is found to be mediated by the frontal-limbic neural circuits. However, the correlations between PE and emotion are still unclear.

          Methods

          Resting-state functional magnetic resonance imaging (rs-fMRI) data were acquired in 27 PE patients with stable emotion (SPE), 27 PE patients with abnormal emotion (NPE), and 30 healthy controls (HC). We used rs-fMRI to explore the underlying neural mechanisms in SPE, NPE, and HC by measuring the functional connectivity (FC). Differences of FC values among the three groups were compared when choosing bilateral amygdala as the regions of interest (ROIs). We also explored the correlations between the brain regions showing altered FC values and scores of the premature ejaculation diagnostic tool (PEDT)/Eysenck Personality Inventory about neuroticism (EPQ-N) in the PE group.

          Results

          When the left amygdala was chosen as the ROI, the SPE group exhibited an increased FC between the left medial superior frontal gyrus (SFGmed) and amygdala compared with the NPE or HC group. When the right amygdala was chosen as the ROI, the NPE group exhibited a decreased FC between the left SFGmed and right amygdala compared with the HC group. In addition, FC values of the left SFGmed had positive correlations with PEDT and negative correlations with EPQ-N scores in the PE group. Moreover, FC values of the left superior temporal gyrus had positive correlations with EPQ-N scores in the PE group.

          Conclusion

          The increased FC values between the left SFGmed and amygdala could reflect a compensatory cortical control mechanism with the effect of stabilized emotion in the limbic regions of PE patients. Abnormal FC between these brain regions could play a critical role in the physiopathology of PE and could help us in dividing PE into more subtypes.

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          Most cited references61

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          DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging.

          Brain imaging efforts are being increasingly devoted to decode the functioning of the human brain. Among neuroimaging techniques, resting-state fMRI (R-fMRI) is currently expanding exponentially. Beyond the general neuroimaging analysis packages (e.g., SPM, AFNI and FSL), REST and DPARSF were developed to meet the increasing need of user-friendly toolboxes for R-fMRI data processing. To address recently identified methodological challenges of R-fMRI, we introduce the newly developed toolbox, DPABI, which was evolved from REST and DPARSF. DPABI incorporates recent research advances on head motion control and measurement standardization, thus allowing users to evaluate results using stringent control strategies. DPABI also emphasizes test-retest reliability and quality control of data processing. Furthermore, DPABI provides a user-friendly pipeline analysis toolkit for rat/monkey R-fMRI data analysis to reflect the rapid advances in animal imaging. In addition, DPABI includes preprocessing modules for task-based fMRI, voxel-based morphometry analysis, statistical analysis and results viewing. DPABI is designed to make data analysis require fewer manual operations, be less time-consuming, have a lower skill requirement, a smaller risk of inadvertent mistakes, and be more comparable across studies. We anticipate this open-source toolbox will assist novices and expert users alike and continue to support advancing R-fMRI methodology and its application to clinical translational studies.
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            Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder.

            Little is known about the neural abnormalities underlying generalized anxiety disorder (GAD). Studies in other anxiety disorders have implicated the amygdala, but work in GAD has yielded conflicting results. The amygdala is composed of distinct subregions that interact with dissociable brain networks, which have been studied only in experimental animals. A functional connectivity approach at the subregional level may therefore yield novel insights into GAD. To determine whether distinct connectivity patterns can be reliably identified for the basolateral (BLA) and centromedial (CMA) subregions of the human amygdala, and to examine subregional connectivity patterns and potential compensatory amygdalar connectivity in GAD. Cross-sectional study. Academic medical center. Two cohorts of healthy control subjects (consisting of 17 and 31 subjects) and 16 patients with GAD. Functional connectivity with cytoarchitectonically determined BLA and CMA regions of interest, measured during functional magnetic resonance imaging performed while subjects were resting quietly in the scanner. Amygdalar gray matter volume was also investigated with voxel-based morphometry. Reproducible subregional differences in large-scale connectivity were identified in both cohorts of healthy controls. The BLA was differentially connected with primary and higher-order sensory and medial prefrontal cortices. The CMA was connected with the midbrain, thalamus, and cerebellum. In GAD patients, BLA and CMA connectivity patterns were significantly less distinct, and increased gray matter volume was noted primarily in the CMA. Across the subregions, GAD patients had increased connectivity with a previously characterized frontoparietal executive control network and decreased connectivity with an insula- and cingulate-based salience network. Our findings provide new insights into the functional neuroanatomy of the human amygdala and converge with connectivity studies in experimental animals. In GAD, we find evidence of an intra-amygdalar abnormality and engagement of a compensatory frontoparietal executive control network, consistent with cognitive theories of GAD.
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              Subregions of the human superior frontal gyrus and their connections.

              The superior frontal gyrus (SFG) is located at the superior part of the prefrontal cortex and is involved in a variety of functions, suggesting the existence of functional subregions. However, parcellation schemes of the human SFG and the connection patterns of each subregion remain unclear. We firstly parcellated the human SFG into the anteromedial (SFGam), dorsolateral (SFGdl), and posterior (SFGp) subregions based on diffusion tensor tractography. The SFGam was anatomically connected with the anterior and mid-cingulate cortices, which are critical nodes of the cognitive control network and the default mode network (DMN). The SFGdl was connected with the middle and inferior frontal gyri, which are involved in the cognitive execution network. The SFGp was connected with the precentral gyrus, caudate, thalamus, and frontal operculum, which are nodes of the motor control network. Resting-state functional connectivity analysis further revealed that the SFGam was mainly correlated with the cognitive control network and the DMN; the SFGdl was correlated with the cognitive execution network and the DMN; and the SFGp was correlated with the sensorimotor-related brain regions. The SFGam and SFGdl were further parcellated into three and two subclusters that are well corresponding to Brodmann areas. These findings suggest that the human SFG consists of multiple dissociable subregions that have distinct connection patterns and that these subregions are involved in different functional networks and serve different functions. These results may improve our understanding on the functional complexity of the SFG and provide us an approach to investigate the SFG at the subregional level. Copyright © 2013 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                29 July 2021
                2021
                : 15
                : 704920
                Affiliations
                [1] 1Department of Andrology, Jiangsu Province Hospital of Chinese Medicine, Affiliated Hospital of Nanjing University of Chinese Medicine , Nanjing, China
                [2] 2Department of Andrology, Yangzhou Traditional Chinese Medicine Hospital, Affiliated to Nanjing University of Chinese Medicine , Nanjing, China
                [3] 3Department of Urology, Jiangsu Provincial People’s Hospital, First Affiliated Hospital of Nanjing Medical University , Nanjing, China
                [4] 4Department of Urology, People’s Hospital of Xinjiang Kizilsu Kirgiz Autonomous Prefecture , Ürümqi, China
                Author notes

                Edited by: Xiao Liu, The Pennsylvania State University (PSU), United States

                Reviewed by: Anubha Gupta, Indraprastha Institute of Information Technology Delhi, India; Manxiu Ma, Virginia Tech Carilion, United States

                *Correspondence: Jianhuai Chen, jianhuaichen@ 123456126.com

                These authors share first authorship

                This article was submitted to Brain Imaging Methods, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2021.704920
                8375680
                34421524
                017d0c5e-f03e-4184-8e7a-7124f75773db
                Copyright © 2021 Xu, Zhang, Xiang, Wang, Huang, Liu, Yang, Chen, Xue, Chen and Yang.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 04 May 2021
                : 28 June 2021
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 61, Pages: 11, Words: 0
                Categories
                Neuroscience
                Original Research

                Neurosciences
                premature ejaculation,resting-state functional magnetic resonance imaging,functional connectivity,emotion,amygdala

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