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      Connectivity of precuneus to the default mode and dorsal attention networks: A possible invariant marker of long-term tinnitus

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          Abstract

          Resting state functional connectivity studies of tinnitus have provided inconsistent evidence concerning its neural bases. This may be due to differences in the methodology used, but it is also likely related to the heterogeneity of the tinnitus population. In this study, our goal was to identify resting state functional connectivity alterations that consistently appear across tinnitus subgroups. We examined two sources of variability in the subgroups: tinnitus severity and the length of time a person has had chronic tinnitus (referred to as tinnitus duration). Data for the current large-scale analysis of variance originated partly from our earlier investigations (Schmidt et al., 2013; Carpenter-Thompson et al., 2015) and partly from previously unpublished studies. Decreased correlations between seed regions in the default mode network and the precuneus were consistent across individuals with long-term tinnitus (who have had tinnitus for greater than one year), with more bothersome tinnitus demonstrating stronger decreases. In the dorsal attention network, patients with moderately severe tinnitus showed increased correlations between seeds in the network and the precuneus, with this effect also present in only some patients with mild tinnitus. The same effects were not seen in patients with mild tinnitus and tinnitus duration between 6 and 12 months. Our results are promising initial steps towards identifying invariant neural correlates of tinnitus and indexing differences between subgroups.

          Highlights

          • Resting state functional connectivity in tinnitus subgroups was examined.

          • Default mode network showed decreased correlation to precuneus in long-term tinnitus.

          • Dorsal attention network had stronger correlation to precuneus in bothersome tinnitus.

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          Most cited references36

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          Reorganization of brain networks in aging: a review of functional connectivity studies

          Healthy aging (HA) is associated with certain declines in cognitive functions, even in individuals that are free of any process of degenerative illness. Functional magnetic resonance imaging (fMRI) has been widely used in order to link this age-related cognitive decline with patterns of altered brain function. A consistent finding in the fMRI literature is that healthy old adults present higher activity levels in some brain regions during the performance of cognitive tasks. This finding is usually interpreted as a compensatory mechanism. More recent approaches have focused on the study of functional connectivity, mainly derived from resting state fMRI, and have concluded that the higher levels of activity coexist with disrupted connectivity. In this review, we aim to provide a state-of-the-art description of the usefulness and the interpretations of functional brain connectivity in the context of HA. We first give a background that includes some basic aspects and methodological issues regarding functional connectivity. We summarize the main findings and the cognitive models that have been derived from task-activity studies, and we then review the findings provided by resting-state functional connectivity in HA. Finally, we suggest some future directions in this field of research. A common finding of the studies included is that older subjects present reduced functional connectivity compared to young adults. This reduced connectivity affects the main brain networks and explains age-related cognitive alterations. Remarkably, the default mode network appears as a highly compromised system in HA. Overall, the scenario given by both activity and connectivity studies also suggests that the trajectory of changes during task may differ from those observed during resting-state. We propose that the use of complex modeling approaches studying effective connectivity may help to understand context-dependent functional reorganizations in the aging process.
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            Development of the Tinnitus Handicap Inventory.

            To develop a self-report tinnitus handicap measure that is brief, easy to administer and interpret, broad in scope, and psychometrically robust. A standardization study of a self-report tinnitus handicap measure was conducted to determine its internal consistency reliability and convergent and construct validity. Audiology clinics in tertiary care centers in two sites. In the first investigation, 84 patients reporting tinnitus as their primary complaint or secondary to hearing loss completed the 45-item alpha version of the Tinnitus Handicap Inventory (THI). In the second investigation, 66 subjects also reporting tinnitus completed the 25-item beta version. Convergent validity was assessed using another measure of perceived tinnitus handicap (Tinnitus Handicap Questionnaire). Construct validity was assessed using the Beck Depression Inventory, Modified Somatic Perception Questionnaire, symptom rating scales (annoyance, sleep disruption, depression, and concentration), and perceived tinnitus pitch and loudness judgments. From the alpha version of the THI, we derived a 25-item beta version with the items grouped into functional, emotional, and catastrophic subscales. The total scale yielded excellent internal consistency reliability (Cronbach's alpha = .93). No significant age or gender effects were seen. Weak correlations were observed between the THI and the Beck Depression Inventory, Modified Somatic Perception Questionnaire, and pitch and loudness judgments. Significant correlations were found between the THI and the symptom rating scales. The THI is a self-report measure that can be used in a busy clinical practice to quantify the impact of tinnitus on daily living.
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              Two distinct neuronal networks mediate the awareness of environment and of self.

              Evidence from functional neuroimaging studies on resting state suggests that there are two distinct anticorrelated cortical systems that mediate conscious awareness: an "extrinsic" system that encompasses lateral fronto-parietal areas and has been linked with processes of external input (external awareness), and an "intrinsic" system which encompasses mainly medial brain areas and has been associated with internal processes (internal awareness). The aim of our study was to explore the neural correlates of resting state by providing behavioral and neuroimaging data from healthy volunteers. With no a priori assumptions, we first determined behaviorally the relationship between external and internal awareness in 31 subjects. We found a significant anticorrelation between external and internal awareness with a mean switching frequency of 0.05 Hz (range: 0.01-0.1 Hz). Interestingly, this frequency is similar to BOLD fMRI slow oscillations. We then evaluated 22 healthy volunteers in an fMRI paradigm looking for brain areas where BOLD activity correlated with "internal" and "external" scores. Activation of precuneus/posterior cingulate, anterior cingulate/mesiofrontal cortices, and parahippocampal areas ("intrinsic system") was linearly linked to intensity of internal awareness, whereas activation of lateral fronto-parietal cortices ("extrinsic system") was linearly associated with intensity of external awareness.
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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                22 July 2017
                2017
                22 July 2017
                : 16
                : 196-204
                Affiliations
                [a ]Neuroscience Program, University of Illinois, Champaign, IL 61820, USA
                [b ]Department of Speech and Hearing Science, University of Illinois, Champaign, IL 61820, USA
                [c ]College of Medicine, University of Illinois, Champaign, IL 61820, USA
                [d ]Beckman Institute for Advanced Science and Technology, University of Illinois, Champaign, IL 61820, USA
                Author notes
                [* ]Corresponding author at: 901 S Sixth Street, Champaign, IL 61820, USA.901 S Sixth StreetChampaignIL61820USA saschmi3@ 123456illinois.edu
                Article
                S2213-1582(17)30180-8
                10.1016/j.nicl.2017.07.015
                5542421
                28794980
                99337406-8ba3-48a7-ac93-b0576e0536a3
                © 2017 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 9 May 2017
                : 14 July 2017
                : 20 July 2017
                Categories
                Regular Article

                tinnitus,resting state functional connectivity,fmri,default mode network,dorsal attention network,precuneus

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