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      Disrupted Intraregional Brain Activity and Functional Connectivity in Unilateral Acute Tinnitus Patients With Hearing Loss

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          Abstract

          Purpose

          The present study combined fractional amplitude of low-frequency fluctuations (fALFF), regional homogeneity (ReHo), and functional connectivity (FC) to explore brain functional abnormalities in acute tinnitus patients (AT) with hearing loss.

          Methods

          We recruited twenty-eight AT patients and 31 healthy controls (HCs) and ran resting-state functional magnetic resonance imaging (fMRI) scans. fALFF, ReHo, and FC were conducted and compared between AT patients and HCs. After that, we calculated correlation analyses among abnormal fALFF, ReHo, FC, and clinical data in AT patients.

          Results

          Compared with HCs, AT showed increased fALFF values in the right inferior temporal gyrus (ITG). In contrast, significantly decreased ReHo values were observed in the cerebellar vermis, the right calcarine cortex, the right precuneus, the right supramarginal gyrus (SMG), and the right middle frontal gyrus (MFG). Based on the differences in the fALFF and ReHo maps, the latter of which we defined as region-of-interest (ROI) for FC analysis, the right ITG exhibited increased connectivity with the right precentral gyrus. In addition, the right MFG demonstrated decreased connectivity with both the bilateral anterior cingulate cortex (ACC) and the left precentral gyrus.

          Conclusion

          By combining ReHo, fALFF, and FC analyses, our work indicated that AT with hearing loss had abnormal intraregional neural activity and disrupted connectivity in several brain regions which mainly involving the non-auditory area, and these regions are major components of default mode network (DMN), attention network, visual network, and executive control network. These findings will help us enhance the understanding of the neuroimaging mechanism in tinnitus populations. Moreover, these abnormalities remind us that we should focus on the early stages of this hearing disease.

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          Most cited references63

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          From sensation to cognition.

          M. Mesulam (1998)
          Sensory information undergoes extensive associative elaboration and attentional modulation as it becomes incorporated into the texture of cognition. This process occurs along a core synaptic hierarchy which includes the primary sensory, upstream unimodal, downstream unimodal, heteromodal, paralimbic and limbic zones of the cerebral cortex. Connections from one zone to another are reciprocal and allow higher synaptic levels to exert a feedback (top-down) influence upon earlier levels of processing. Each cortical area provides a nexus for the convergence of afferents and divergence of efferents. The resultant synaptic organization supports parallel as well as serial processing, and allows each sensory event to initiate multiple cognitive and behavioural outcomes. Upstream sectors of unimodal association areas encode basic features of sensation such as colour, motion, form and pitch. More complex contents of sensory experience such as objects, faces, word-forms, spatial locations and sound sequences become encoded within downstream sectors of unimodal areas by groups of coarsely tuned neurons. The highest synaptic levels of sensory-fugal processing are occupied by heteromodal, paralimbic and limbic cortices, collectively known as transmodal areas. The unique role of these areas is to bind multiple unimodal and other transmodal areas into distributed but integrated multimodal representations. Transmodal areas in the midtemporal cortex, Wernicke's area, the hippocampal-entorhinal complex and the posterior parietal cortex provide critical gateways for transforming perception into recognition, word-forms into meaning, scenes and events into experiences, and spatial locations into targets for exploration. All cognitive processes arise from analogous associative transformations of similar sets of sensory inputs. The differences in the resultant cognitive operation are determined by the anatomical and physiological properties of the transmodal node that acts as the critical gateway for the dominant transformation. Interconnected sets of transmodal nodes provide anatomical and computational epicentres for large-scale neurocognitive networks. In keeping with the principles of selectively distributed processing, each epicentre of a large-scale network displays a relative specialization for a specific behavioural component of its principal neurospychological domain. The destruction of transmodal epicentres causes global impairments such as multimodal anomia, neglect and amnesia, whereas their selective disconnection from relevant unimodal areas elicits modality-specific impairments such as prosopagnosia, pure word blindness and category-specific anomias. The human brain contains at least five anatomically distinct networks. The network for spatial awareness is based on transmodal epicentres in the posterior parietal cortex and the frontal eye fields; the language network on epicentres in Wernicke's and Broca's areas; the explicit memory/emotion network on epicentres in the hippocampal-entorhinal complex and the amygdala; the face-object recognition network on epicentres in the midtemporal and temporopolar cortices; and the working memory-executive function network on epicentres in the lateral prefrontal cortex and perhaps the posterior parietal cortex. Individual sensory modalities give rise to streams of processing directed to transmodal nodes belonging to each of these networks. The fidelity of sensory channels is actively protected through approximately four synaptic levels of sensory-fugal processing. The modality-specific cortices at these four synaptic levels encode the most veridical representations of experience. Attentional, motivational and emotional modulations, including those related to working memory, novelty-seeking and mental imagery, become increasingly more pronounced within downstream components of unimodal areas, where they help to create a highly edited subjective version of the world. (ABSTRACT TRUNCATED)
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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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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                19 September 2019
                2019
                : 13
                : 1010
                Affiliations
                [1] 1Department of Radiology, The Affiliated Jiangning Hospital of Nanjing Medical University , Nanjing, China
                [2] 2Department of ENT, The Affiliated Jiangning Hospital of Nanjing Medical University , Nanjing, China
                [3] 3Department of Radiology, Nanjing First Hospital, Nanjing Medical University , Nanjing, China
                Author notes

                Edited by: Jae-Jin Song, Seoul National University Bundang Hospital, South Korea

                Reviewed by: Paul T. Fillmore, Baylor University, United States; Gaoxiong Duan, Guangxi University of Chinese Medicine, China; Haijun Li, Nanchang University, China

                *Correspondence: Hong Zhang, jnyyfsk@ 123456126.com

                These authors have contributed equally to this work

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

                Article
                10.3389/fnins.2019.01010
                6761222
                31607851
                e8e978d6-053c-48d9-aa1c-95159dad0417
                Copyright © 2019 Zhou, Shi, Wei, Qu, Yu, Zhou, Yin, Zhang and Tao.

                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
                : 09 May 2019
                : 05 September 2019
                Page count
                Figures: 4, Tables: 4, Equations: 0, References: 77, Pages: 10, Words: 0
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 81601477
                Categories
                Neuroscience
                Original Research

                Neurosciences
                tinnitus,fmri,falff,reho,fc,dmn
                Neurosciences
                tinnitus, fmri, falff, reho, fc, dmn

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