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Maladaptive alterations of resting state cortical network in Tinnitus: A directed functional connectivity analysis of a larger MEG data set.

Published on Oct 29, 2019in Scientific Reports4.011
· DOI :10.1038/S41598-019-51747-Z
Evangelos Paraskevopoulos11
Estimated H-index: 11
(A.U.Th.: Aristotle University of Thessaloniki),
Christian Dobel21
Estimated H-index: 21
+ 3 AuthorsChristo Pantev63
Estimated H-index: 63
(WWU: University of Münster)
Abstract
The present study used resting state MEG whole-head recordings to identify how chronic tonal tinnitus relates to altered functional connectivity of brain’s intrinsic cortical networks. Resting state MEG activity of 40 chronic tinnitus patients and 40 matched human controls was compared identifying significant alterations in intrinsic networks of the tinnitus population. Directed functional connectivity of the resting brain, at a whole cortex level, was estimated by means of a statistical comparison of the estimated phase Transfer Entropy (pTE) between the time-series of cortical activations, as reconstructed by LORETA. As pTE identifies the direction of the information flow, a detailed analysis of the connectivity differences between tinnitus patients and controls was possible. Results indicate that the group of tinnitus patients show increased connectivity from right dorsal prefrontal to right medial temporal areas. Our results go beyond previous findings by indicating that the role of the left para-hippocampal area is dictated by a modulation from dmPFC; a region that is part of the dorsal attention network (DAN), as well as implicated in the regulation of emotional processing. Additionally, this whole cortex analysis showed a crucial role of the left inferior parietal cortex, which modulated the activity of the right superior temporal gyrus, providing new hypotheses for the role of this area within the context of current tinnitus models. Overall, these maladaptive alterations of the structure of intrinsic cortical networks show a decrease in efficiency and small worldness of the resting state network of tinnitus patients, which is correlated to tinnitus distress.
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References71
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#1Anusha Mohan (UTD: University of Texas at Dallas)H-Index: 5
#2Christian Davidson (UTSW: University of Texas Southwestern Medical Center)H-Index: 1
Last. Sven Vanneste (UTD: University of Texas at Dallas)H-Index: 44
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Tinnitus, the perception of a phantom sound, is accompanied by loudness and distress components. Distress however accompanies not just tinnitus, but several disorders. Several functional connectivity studies show that distress is characterized by disconnectivity of fronto-limbic circuits or hyperconnectivity of default mode/salience networks. The drawback, however, is that it considers only the magnitude of connectivity, not the direction. Thus, the current study aims to identify the core networ...
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#1Pia LauH-Index: 7
#2Andreas WollbrinkH-Index: 15
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Abstract Tinnitus is a prevalent phenomenon and bothersome for people affected by it. Its occurrence and maintenance have a clear neuroscientific tie and one aspect are differences in the neuronal oscillatory pattern, especially in auditory cortical areas. As studies in this field come to different results, the aim of this study was to analyze a large number of participants to achieve more stable results. Furthermore, we expanded our analysis to two variables of potential influence, namely being...
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#1Rodrigo Araneda (UCL: Université catholique de Louvain)H-Index: 6
#2Laurent Renier (UCL: Université catholique de Louvain)H-Index: 16
Last. Anne De Volder (UCL: Université catholique de Louvain)H-Index: 24
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Abstract Introduction Since we recently showed in behavioural tasks that the top-down cognitive control was specifically altered in tinnitus sufferers, here we wanted to establish the link between this impaired executive function and brain alterations in the frontal cortex in tinnitus patients. Method Using functional magnetic resonance imaging (fMRI), we monitored the brain activity changes in sixteen tinnitus patients (TP) and their control subjects (CS) while they were performing a spatial St...
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#1Danielle S. Bassett (UPenn: University of Pennsylvania)H-Index: 60
#2Edward T. Bullmore (University of Cambridge)H-Index: 147
It is nearly 20 years since the concept of a small-world network was first quantitatively defined, by a combination of high clustering and short path length; and about 10 years since this metric of complex network topology began to be widely applied to analysis of neuroimaging and other neuroscience data as part of the rapid growth of the new field of connectomics. Here, we review briefly the foundational concepts of graph theoretical estimation and generation of small-world networks. We take st...
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#2Stefan Bode (University of Melbourne)H-Index: 21
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: The ability to voluntarily regulate our emotional response to threatening and highly arousing stimuli by using cognitive reappraisal strategies is essential for our mental and physical well-being. This might be achieved by prefrontal brain regions (e.g. inferior frontal gyrus, IFG) down-regulating activity in the amygdala. It is unknown, to which degree effective connectivity within the emotion-regulation network is linked to individual differences in reappraisal skills. Using psychophysiologi...
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#1Yu-Chen Chen (Nanjing Medical University)H-Index: 9
#2Fang Wang (Nanjing Medical University)H-Index: 2
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Purpose: The neural mechanisms that give rise to the phantom sound of tinnitus have not been fully elucidated. Neuroimaging studies have revealed abnormalities in resting-state activity that could represent the neural signature of tinnitus, but there is considerable heterogeneity in the data. To address this issue, we conducted a meta-analysis of published neuroimaging studies aimed at identifying a common core of resting-state brain abnormalities in tinnitus patients. Methods: A systematic sear...
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#2Wenqing Xia (Nanjing Medical University)H-Index: 9
Last. Xindao Yin (Nanjing Medical University)H-Index: 6
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The phantom sound of tinnitus is believed to be triggered by aberrant neural activity in the central auditory pathway, but since this debilitating condition is often associated with emotional distress and anxiety, these comorbidities likely arise from maladaptive functional connections to limbic structures such as the amygdala and hippocampus. To test this hypothesis, resting-state functional magnetic resonance imaging (fMRI) was used to identify aberrant effective connectivity of the amygdala a...
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#1Sara A. Schmidt (UIUC: University of Illinois at Urbana–Champaign)H-Index: 9
#2Jake R. Carpenter-Thompson (UIUC: University of Illinois at Urbana–Champaign)H-Index: 7
Last. Fatima T. Husain (UIUC: University of Illinois at Urbana–Champaign)H-Index: 18
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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 o...
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#2Karl J. Friston (Wellcome Trust Centre for Neuroimaging)H-Index: 193
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Tinnitus is a common disorder that often complicates hearing loss. Its mechanisms are incompletely understood. Current theories proposing pathophysiology from the ear to the cortex cannot individually – or collectively – explain the range of experimental evidence available. We propose a new framework, based on predictive coding, in which spontaneous activity in the subcortical auditory pathway constitutes a ‘tinnitus precursor' which is normally ignored as imprecise evidence against the prevaili...
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Importance Tinnitus is a common problem for millions of individuals and can cause substantial negative effects on their quality of life. A large epidemiologic study of tinnitus and its management patterns in the US adult population is lacking. Objectives To quantify the epidemiologic features and effect of tinnitus and to analyze the management of tinnitus in the United States relative to the 2014 American Academy of Otolaryngology–Head and Neck Surgery Foundation (AAO-HNSF) clinical practice gu...
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