Tinnitus and the Triple Network Model: A Perspective

BMC Neuroscience, 2012

Background: The objective was to examine functional connectivity linked to the auditory system in patients with bothersome tinnitus. Activity was low frequency (< 0.1 Hz), spontaneous blood oxygenation level-dependent (BOLD) responses at rest. The question was whether the experience of chronic bothersome tinnitus induced changes in synaptic efficacy between co-activated components. Functional connectivity for seed regions in auditory, visual, attention, and control networks was computed across all 2 mm 3 brain volumes in 17 patients with moderate-severe bothersome tinnitus (Tinnitus Handicap Index: average 53.5 ± 3.6 (range 38-76)) and 17 agematched controls. Results: In bothersome tinnitus, negative correlations reciprocally characterized functional connectivity between auditory and occipital/visual cortex. Negative correlations indicate that when BOLD response magnitudes increased in auditory or visual cortex they decreased in the linked visual or auditory cortex, suggesting reciprocally phase reversed activity between functionally connected locations in tinnitus. Both groups showed similar connectivity with positive correlations within the auditory network. Connectivity for primary visual cortex in tinnitus included extensive negative correlations in the ventral attention temporoparietal junction and in the inferior frontal gyrus and rostral insula -executive control network components. Rostral insula and inferior frontal gyrus connectivity in tinnitus also showed greater negative correlations in occipital cortex.

2018

Background and Aim: Tinnitus, the phantom perception of sound, in which many cortical and subcortical areas are involved has become one of the popular subjects of neuroscience research. Neuroimaging studies have introduced the tinnitus network model to explain the involvement of auditory and non-auditory areas in this perception. In such a model, the cognitive and emotional aspects of tinnitus can be interpreted conveniently. Therefore, this paper aimed to review the neural basis of tinnitus networks, including data from neuroimaging studies, and discuss the clinical implication of this concept, as well. Recent Findings: The data from neuroimaging studies were reviewed and discussed in order to complete the overall image of tinnitus network and its correlates such as the distress network, attentional network and other cognitive mechanisms. In addition to the auditory system, the anterior cingulate cortex (ACC) and dorsolateral prefrontal cortex (DLPFC) were considered to be important hubs in tinnitus distress network, especially for having important connectivity

Scientific Reports, 2019

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 parahippocampal 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. Chronic tinnitus is the experience of a persistent auditory phantom percept, being heard in the absence of an external source for a period of time longer than three months 1. It affects 9-15% of the general population, while a subtle, transient tinnitus percept has a prevalence of more than 30% 2,3. The continuity of tinnitus percept is related to significant distress and reduction in quality of life, accompanied by sleeping problems, stress, depression and substance abuse 4. Several models have been proposed in order to explain the factors that generate tinnitus 5-8 , highlighting its association with maladaptive subcortical and cortical processes such as hyperactivity, burst firing and hyper-synchronicity, following hearing loss 9. Nonetheless, our understanding of its underlying physiological mechanisms remains insufficient, while recent evidence suggests that the percept of tinnitus is linked with altered interaction between intrinsic cortical networks 10-12. The initial generation of this phantom, but extremely bothersome percept is thought to be caused by damage to the auditory periphery, leading to functional de-afferentation of the tonotopically arranged auditory neurons 13. The de-afferented neurons start to respond preferentially to frequencies neighboring the hearing loss region, resulting in reduced lateral inhibition onto neurons coding the audiometric edge. Maladaptive plasticity processes follow, reorganizing the tonotopic structure to compensate the lack of lateral inhibition 8,14. This working model of tinnitus, partially confirmed in animal studies 15 , does not fully explain its chronification, nor the discomfort caused by tinnitus. Instead, findings related to the contribution of emotional and attentional processes 12,16 ,

Investigative Magnetic Resonance Imaging

One of the suggested potential mechanisms of tinnitus is an alteration in perception in the neural auditory pathway. The aim of this study was to investigate the difference in laterality in functional connectivity between tinnitus patients and healthy controls using resting state functional MRI (rs-fMRI). Materials and Methods: Thirty-eight chronic tinnitus subjects and 45 age-matched healthy controls were enrolled in this study. Connectivity was investigated using independent component analysis, and the laterality index map was calculated based on auditory (AN) and dorsal attention (DAN), default mode (DMN), sensorimotor, salience (SalN), and visual networks (VNs). The laterality index (LI) of tinnitus subjects was compared with that of normal controls using region-of-interest (ROI) and voxelbased methods and a two-sample unpaired t-test. Pearson correlation was conducted to assess the associations between the LI in each network and clinical variables. Results: The AN and VN showed significant differences in LI between the two groups in ROI analysis (P < 0.05), and the tinnitus group had clusters with significantly decreased laterality of AN, SalN, and VN in voxel-based comparisons. The AN was positively correlated with tinnitus distress (tinnitus handicap inventory), and the SalN was negatively correlated with symptom duration (P < 0.05). Conclusion: The results of this study suggest that various functional networks related to psychological distress can be modified by tinnitus, and that this interrelation can present differently on the right and left sides, according to the dominance of the network.

Frontiers in Neuroscience, 2016

Advances in experimental medicine and biology, 2016

We investigated tinnitus-related differences in functional networks in adults with tinnitus by means of a functional connectivity study. Previously it was found that various networks show differences in connectivity in patients with tinnitus compared to controls. How this relates to patients&#39; ongoing tinnitus and whether the ecological sensory environment modulates connectivity remains unknown.Twenty healthy controls and twenty patients suffering from chronic tinnitus were enrolled in this study. Except for the presence of tinnitus in the patient group, all subjects were selected to have normal or near-normal hearing. fMRI data were obtained in two different functional states. In one set of runs, subjects freely viewed emotionally salient movie fragments (&quot;fixed-state&quot;) while in the other they were not performing any task (&quot;resting-state&quot;). After data pre-processing, Principal Component Analysis was performed to obtain 25 components for all datasets. These we...

Scientific reports, 2017

Tinnitus (ringing in the ears) is a common auditory sensation that can become a chronic debilitating health condition with pervasive effects on health and wellbeing, substantive economic burden, and no known cure. Here we investigate if impaired functioning of the cognitive control network that directs attentional focus is a mechanism erroneously maintaining the tinnitus sensation. Fifteen people with chronic tinnitus and 15 healthy controls matched for age and gender from the community performed a cognitively demanding task known to activate the cognitive control network in this functional magnetic resonance imaging study. We identify attenuated activation of a core node of the cognitive control network (the right middle frontal gyrus), and altered baseline connectivity between this node and nodes of the salience and autobiographical memory networks. Our findings indicate that in addition to auditory dysfunction, altered interactions between non-auditory neurocognitive networks mai...

Hearing Research, 2013

Chronic tinnitus affects approximately 5% of the population. Severe distress due to the phantom noise is experienced by 20% of the tinnitus patients. This distress cannot be predicted by psychoacoustic features of the tinnitus. It is commonly assumed that negative cognitive emotional evaluation of the tinnitus and its expected consequences is a major factor that determines the impact of tinnitus-related distress. Models of tinnitus distress and recently conducted research propose differences in limbic, frontal and parietal processing between highly and low distressed tinnitus patients. An experimental paradigm using verbal material to stimulate cognitive emotional processing of tinnitus-related information was conducted. Age and sex matched highly (n ¼ 16) and low (n ¼ 16) distressed tinnitus patients and healthy controls (n ¼ 16) underwent functional magnetic resonance imaging (fMRI) while sentences with neutral, negative or tinnitus-related content were presented. A random effects group analysis was performed on the basis of the general linear model. Tinnitus patients showed stronger activations to tinnitus-related sentences in comparison to neutral sentences than healthy controls in various limbic/ emotion processing areas, such as the anterior cingulate cortex, midcingulate cortex, posterior cingulate cortex, retrosplenial cortex and insula and also in frontal areas. Highly and low distressed tinnitus patients differed in terms of activation of the left middle frontal gyrus. A connectivity analysis and correlational analysis between the predictors of the general linear model of relevant contrasts and tinnitus-related distress further supported the idea of a fronto-parietal-cingulate network, which seems to be more active in highly distressed tinnitus patients. This network may present an aspecific distress network. Based on the findings the left middle frontal gyrus and the right medial frontal gyrus are suggested as target regions for neuromodulatory approaches in the treatment of tinnitus. For future studies we recommend the use of idiosyncratic stimulus material.

Frontiers in Systems Neuroscience, 2012

2007

Tinnitus refers to the persistent sensation of sound in the absence of a corresponding physical source. We suggest that both the perceptual and the affective aspects of this phantom sensation arise from a distributed cerebral network whereby the functional coupling between neural nodes involved would be realised through phase-synchrony of neural oscillations. In this study, we sought to excite this network by driving it with a 37 Hz amplitude-modulated sound using a carrier frequency similar to the individual tinnitus ringing. Phase coherence measures between different cortical regions revealed significant differences in the excitable network between 12 tinnitus and 10 control subjects. The alterations in tinnitus were closely related to the subjective tinnitus distress ratings and resembled the patterns that have been reported for focused auditory attention.