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      Increased striatal functional connectivity with auditory cortex in tinnitus

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          Abstract

          Tinnitus is a common auditory perceptual disorder whose neural substrates are under intense debate. One physiologically based model posits the dorsal striatum to play a key role in gating auditory phantoms to perceptual awareness. Here, we directly test this model along with the roles of auditory and auditory-limbic networks in tinnitus non-invasively by comparing resting-state fMRI functional connectivity patterns in chronic tinnitus patients against matched control subjects without hearing loss. We assess resting-state functional connectivity of the caudate dorsal striatum (area LC), caudate head (CH), nucleus accumbens (NA), and primary auditory cortex (A1) to determine patterns of abnormal connectivity. In chronic tinnitus, increases in ipsilateral striatal–auditory cortical connectivity are found consistently only in area LC. Other patterns of increased connectivity are as follows: (1) right striatal area LC, A1, CH, and NA with parietal cortex, (2) left and right CHs with dorsal pre-frontal cortex, (3) NA and A1 with cerebellum, hippocampus, visual and ventral pre-frontal cortex. Those findings provide further support for a striatal gating model of tinnitus, where dysfunctionally permissive area LC enables auditory phantoms to reach perceptual awareness.

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          Most cited references47

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          Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization.

          Resting state functional connectivity MRI (fcMRI) is widely used to investigate brain networks that exhibit correlated fluctuations. While fcMRI does not provide direct measurement of anatomic connectivity, accumulating evidence suggests it is sufficiently constrained by anatomy to allow the architecture of distinct brain systems to be characterized. fcMRI is particularly useful for characterizing large-scale systems that span distributed areas (e.g., polysynaptic cortical pathways, cerebro-cerebellar circuits, cortical-thalamic circuits) and has complementary strengths when contrasted with the other major tool available for human connectomics-high angular resolution diffusion imaging (HARDI). We review what is known about fcMRI and then explore fcMRI data reliability, effects of preprocessing, analysis procedures, and effects of different acquisition parameters across six studies (n = 98) to provide recommendations for optimization. Run length (2-12 min), run structure (1 12-min run or 2 6-min runs), temporal resolution (2.5 or 5.0 s), spatial resolution (2 or 3 mm), and the task (fixation, eyes closed rest, eyes open rest, continuous word-classification) were varied. Results revealed moderate to high test-retest reliability. Run structure, temporal resolution, and spatial resolution minimally influenced fcMRI results while fixation and eyes open rest yielded stronger correlations as contrasted to other task conditions. Commonly used preprocessing steps involving regression of nuisance signals minimized nonspecific (noise) correlations including those associated with respiration. The most surprising finding was that estimates of correlation strengths stabilized with acquisition times as brief as 5 min. The brevity and robustness of fcMRI positions it as a powerful tool for large-scale explorations of genetic influences on brain architecture. We conclude by discussing the strengths and limitations of fcMRI and how it can be combined with HARDI techniques to support the emerging field of human connectomics.
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            Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis.

            Recent neuroimaging studies have lead to the proposal that rest is characterized by an organized, baseline level of activity, a default mode of brain function that is suspended during specific goal-oriented mental activity. Previous studies have shown that the primary function subserved by the default mode is that of an introspectively oriented, self-referential mode of mental activity. The default mode of brain function hypothesis is readdressed from the perspective of the presence of low-frequency blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) signal changes (0.012-0.1 Hz) in the resting brain. The results show that the brain during rest is not tonically active in a single mode of brain function. Rather, the findings presented here suggest that the brain recurrently toggles between an introspectively oriented mode (default mode) and a state-of-mind that tentatively might be interpreted as an extrospectively oriented mode that involves a readiness and alertness to changes in the external and internal environment.
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              Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop.

              This paper reviews some of the recent findings on different aspects of the anatomical organization of the basal ganglia. Attempts have been made to delineate the anatomical substrate of information processing along the cortico-basal ganglia-thalamo-cortical loop. Emphasis has been placed on data obtained with highly sensitive anterograde tract-tracing methods applied to the study of the main axis of the loop, which is composed of the striatum, the pallidum, and the substantia nigra. These findings have highlighted the complexities of the organization of the intrinsic basal ganglia circuitry, which comprises multiple modular units that are distributed according to highly ordered and repetitive patterns. Such an arrangement is well suited to convey cortical information in a highly specific manner throughout the basal ganglia. The basal ganglia circuitry is also designed so as to modulate in a precise manner the neuronal activity of several brain functional systems, which are involved in the direct control of different aspects of psychomotor behavior. Of utmost importance is the action of the basal ganglia on thalamocortical premotor neurons. It is through these neurons, which can be considered as a sort of final common pathway, that the basal ganglia ultimately influence the complex neuronal computation that goes on at cortical level.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                28 October 2015
                2015
                : 9
                : 568
                Affiliations
                [1] 1Department of Radiology and Biomedical Imaging, University of California at San Francisco, San Francisco CA, USA
                [2] 2Department of Community Health Systems, School of Nursing, University of California at San Francisco, San Francisco CA, USA
                [3] 3Department of Otolaryngology-Head and Neck Surgery, University of California at San Francisco, San Francisco CA, USA
                [4] 4Surgical Services, San Francisco Veterans Affairs Medical Center, San Francisco CA, USA
                Author notes

                Edited by: John J. Foxe, Albert Einstein College of Medicine, USA

                Reviewed by: Nathan Weisz, University of Trento, Italy; Berthold Langguth, University of Regensburg, Germany; Agnès Job, IRBA-Biomedical Research Institute of the Army, France

                *Correspondence: Steven W. Cheung, steven.cheung@ 123456ucsf.edu ; Srikantan S. Nagarajan, sri@ 123456ucsf.edu
                Article
                10.3389/fnhum.2015.00568
                4623204
                23118abb-0bcd-42c4-a42d-14c63bbf4935
                Copyright © 2015 Hinkley, Mizuiri, Hong, Nagarajan and Cheung.

                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
                : 08 April 2015
                : 28 September 2015
                Page count
                Figures: 5, Tables: 2, Equations: 0, References: 56, Pages: 10, Words: 0
                Funding
                Funded by: Department of Defense 10.13039/100000005
                Award ID: W81XWH-13-1-0494
                Funded by: UCSF Academic Senate Committee 10.13039/100008069
                Funded by: Hearing Research Inc.
                Categories
                Neuroscience
                Original Research

                Neurosciences
                resting-state fmri,tinnitus,striatum,auditory cortex,functional connectivity
                Neurosciences
                resting-state fmri, tinnitus, striatum, auditory cortex, functional connectivity

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