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      Abnormal Resting-State Functional Connectivity of the Anterior Cingulate Cortex in Unilateral Chronic Tinnitus Patients

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          Abstract

          Purpose: The anterior cingulate cortex (ACC) has been suggested to be involved in chronic subjective tinnitus. Tinnitus may arise from aberrant functional coupling between the ACC and cerebral cortex. To explore this hypothesis, we used resting-state functional magnetic resonance imaging (fMRI) to illuminate the functional connectivity (FC) network of the ACC subregions in chronic tinnitus patients.

          Methods: Resting-state fMRI scans were obtained from 31 chronic right-sided tinnitus patients and 40 healthy controls (age, sex, and education well-matched) in this study. Rostral ACC and dorsal ACC were selected as seed regions to investigate the intrinsic FC with the whole brain. The resulting FC patterns were correlated with clinical tinnitus characteristics including the tinnitus duration and tinnitus distress.

          Results: Compared with healthy controls, chronic tinnitus patients showed disrupted FC patterns of ACC within several brain networks, including the auditory cortex, prefrontal cortex, visual cortex, and default mode network (DMN). The Tinnitus Handicap Questionnaires (THQ) scores showed positive correlations with increased FC between the rostral ACC and left precuneus ( r = 0.507, p = 0.008) as well as the dorsal ACC and right inferior parietal lobe ( r = 0.447, p = 0.022).

          Conclusions: Chronic tinnitus patients have abnormal FC networks originating from ACC to other selected brain regions that are associated with specific tinnitus characteristics. Resting-state ACC-cortical FC disturbances may play an important role in neuropathological features underlying chronic tinnitus.

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          Most cited references70

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          Electrophysiological signatures of resting state networks in the human brain.

          Functional neuroimaging and electrophysiological studies have documented a dynamic baseline of intrinsic (not stimulus- or task-evoked) brain activity during resting wakefulness. This baseline is characterized by slow (<0.1 Hz) fluctuations of functional imaging signals that are topographically organized in discrete brain networks, and by much faster (1-80 Hz) electrical oscillations. To investigate the relationship between hemodynamic and electrical oscillations, we have adopted a completely data-driven approach that combines information from simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). Using independent component analysis on the fMRI data, we identified six widely distributed resting state networks. The blood oxygenation level-dependent signal fluctuations associated with each network were correlated with the EEG power variations of delta, theta, alpha, beta, and gamma rhythms. Each functional network was characterized by a specific electrophysiological signature that involved the combination of different brain rhythms. Moreover, the joint EEG/fMRI analysis afforded a finer physiological fractionation of brain networks in the resting human brain. This result supports for the first time in humans the coalescence of several brain rhythms within large-scale brain networks as suggested by biophysical studies.
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            Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations.

            A previous report of correlations in low-frequency resting-state fluctuations between right and left hemisphere motor cortices in rapidly sampled single-slice echoplanar data is confirmed using a whole-body echoplanar MRI scanner at 1.5 T. These correlations are extended to lower sampling rate multislice echoplanar acquisitions and other right/left hemisphere-symmetric functional cortices. The specificity of the correlations in the lower sampling-rate acquisitions is lower due to cardiac and respiratory-cycle effects which are aliased into the pass-band of the low-pass filter. Data are combined for three normal right-handed male subjects. Correlations to left hemisphere motor cortex, visual cortex, and amygdala are measured in long resting-state scans.
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              Phantom auditory perception (tinnitus): mechanisms of generation and perception.

              Phantom auditory perception--tinnitus--is a symptom of many pathologies. Although there are a number of theories postulating certain mechanisms of its generation, none have been proven yet. This paper analyses the phenomenon of tinnitus from the point of view of general neurophysiology. Existing theories and their extrapolation are presented, together with some new potential mechanisms of tinnitus generation, encompassing the involvement of calcium and calcium channels in cochlear function, with implications for malfunction and aging of the auditory and vestibular systems. It is hypothesized that most tinnitus results from the perception of abnormal activity, defined as activity which cannot be induced by any combination of external sounds. Moreover, it is hypothesized that signal recognition and classification circuits, working on holographic or neuronal network-like representation, are involved in the perception of tinnitus and are subject to plastic modification. Furthermore, it is proposed that all levels of the nervous system, to varying degrees, are involved in tinnitus manifestation. These concepts are used to unravel the inexplicable, unique features of tinnitus and its masking. Some clinical implications of these theories are suggested.
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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
                23 January 2018
                2018
                : 12
                : 9
                Affiliations
                [1] 1Department of Radiology, Nanjing First Hospital, Nanjing Medical University , Nanjing, China
                [2] 2Department of Radiology, Beijing Friendship Hospital, Capital Medical University , Beijing, China
                [3] 3Department of Otolaryngology, Nanjing First Hospital, Nanjing Medical University , Nanjing, China
                [4] 4Department of Clinical Laboratory, Nanjing First Hospital, Nanjing Medical University , Nanjing, China
                [5] 5Department of Vascular and Interventional Radiology, Nanjing First Hospital, Nanjing Medical University , Nanjing, China
                Author notes

                Edited by: Victoria M. Bajo Lorenzana, University of Oxford, United Kingdom

                Reviewed by: William Sedley, Newcastle University, United Kingdom; Kathleen A. Garrison, Yale University, United States

                *Correspondence: Shukui Wang sk_wang@ 123456njmu.edu.cn

                This article was submitted to Auditory Cognitive Neuroscience, a section of the journal Frontiers in Neuroscience

                †These authors have contributed equally to this work.

                Article
                10.3389/fnins.2018.00009
                5787069
                29410609
                b2e53ca6-4a74-4204-9270-e0ce96e8db97
                Copyright © 2018 Chen, Liu, Lv, Bo, Feng, Chen, Xu, Yin, Wang and Gu.

                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) or licensor 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
                : 25 October 2017
                : 05 January 2018
                Page count
                Figures: 4, Tables: 2, Equations: 0, References: 85, Pages: 10, Words: 7593
                Categories
                Neuroscience
                Original Research

                Neurosciences
                tinnitus,rostral acc,dorsal acc,functional connectivity,resting-state fmri
                Neurosciences
                tinnitus, rostral acc, dorsal acc, functional connectivity, resting-state fmri

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