Altered networks in bothersome tinnitus: a functional connectivity study

BackgroundThe 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 mm3 brain volumes in 17 patients with moderate-severe bothersome tinnitus (Tinnitus Handicap Index: average 53.5 ± 3.6 (range 38-76)) and 17 age-matched controls.ResultsIn 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.ConclusionsThese results imply that in bothersome tinnitus there is dissociation between activity in auditory cortex and visual, attention and control networks. The reciprocal negative correlations in connectivity between these networks might be maladaptive or reflect adaptations to reduce phantom noise salience and conflict with attention to non-auditory tasks.

[1]  C. Stevens,et al.  Severe tinnitus and its effect on selective and divided attention , 2007, International journal of audiology.

[2]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[3]  M. Corbetta,et al.  Quantitative analysis of attention and detection signals during visual search. , 2003, Journal of neurophysiology.

[4]  T. Elbert,et al.  Reorganization of auditory cortex in tinnitus. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  J. Snow Tinnitus: Theory and Management , 2004 .

[6]  C. Stevens,et al.  Tinnitus and its effect on working memory and attention. , 2006, Journal of speech, language, and hearing research : JSLHR.

[7]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[8]  H. Burton Visual Cortex Activity in Early and Late Blind People , 2003, The Journal of Neuroscience.

[9]  D Baguley,et al.  Guidelines for the grading of tinnitus severity: the results of a working group commissioned by the British Association of Otolaryngologists, Head and Neck Surgeons, 1999. , 2001, Clinical otolaryngology and allied sciences.

[10]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[11]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[12]  H Burton,et al.  Default brain functionality in blind people. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Raichle,et al.  Blood flow changes in human somatosensory cortex during anticipated stimulation , 1995, Nature.

[14]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[15]  M. Corbetta,et al.  Interaction of Stimulus-Driven Reorienting and Expectation in Ventral and Dorsal Frontoparietal and Basal Ganglia-Cortical Networks , 2009, The Journal of Neuroscience.

[16]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[17]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[18]  Andrei G. Vlassenko,et al.  Low-frequency repetitive transcranial magnetic stimulation to the temporoparietal junction for tinnitus. , 2011, Archives of otolaryngology--head & neck surgery.

[19]  J B Spitzer,et al.  Development of the Tinnitus Handicap Inventory. , 1996, Archives of otolaryngology--head & neck surgery.

[20]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[21]  A. Møller The role of neural plasticity in tinnitus. , 2011, Progress in brain research.

[22]  Albert Gjedde,et al.  Positron emission tomography of cortical centers of tinnitus , 1999, Hearing Research.

[23]  D. G. Watts,et al.  Spectral analysis and its applications , 1968 .

[24]  D. Hall,et al.  The mechanisms of tinnitus: Perspectives from human functional neuroimaging , 2009, Hearing Research.

[25]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[26]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[27]  Katherine L. Roberts,et al.  Examining a Supramodal Network for Conflict Processing: A Systematic Review and Novel Functional Magnetic Resonance Imaging Data for Related Visual and Auditory Stroop Tasks , 2008, Journal of Cognitive Neuroscience.

[28]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[29]  Chunshui Yu,et al.  Altered functional connectivity of primary visual cortex in early blindness , 2008, Human brain mapping.

[30]  M. Corbetta,et al.  Right TPJ deactivation during visual search: functional significance and support for a filter hypothesis. , 2007, Cerebral cortex.

[31]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[32]  R. S. Tyler,et al.  Difficulties experienced by tinnitus sufferers. , 1983, The Journal of speech and hearing disorders.

[33]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[34]  J. Henry,et al.  General review of tinnitus: prevalence, mechanisms, effects, and management. , 2005, Journal of speech, language, and hearing research : JSLHR.

[35]  D. Adrian,et al.  The epidemiology of tinnitus , 2000 .

[36]  Jack L. Lancaster,et al.  A modality‐independent approach to spatial normalization of tomographic images of the human brain , 1995 .

[37]  Jeffrey M. Zacks,et al.  Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses , 2006, Nature Neuroscience.

[38]  P. Jastreboff Phantom auditory perception (tinnitus): mechanisms of generation and perception , 1990, Neuroscience Research.

[39]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  Maurizio Corbetta,et al.  The role of impaired neuronal communication in neurological disorders , 2007, Current opinion in neurology.

[41]  D. V. van Essen,et al.  Cortical Folding Abnormalities in Autism Revealed by Surface-Based Morphometry , 2007, The Journal of Neuroscience.

[42]  A. Beck,et al.  An inventory for measuring depression. , 1961, Archives of general psychiatry.

[43]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[44]  A. Møller Similarities between severe tinnitus and chronic pain. , 2000, Journal of the American Academy of Audiology.

[45]  Robert A Dobie,et al.  Depression and tinnitus. , 2003, Otolaryngologic clinics of North America.

[46]  Richard S. Hallam,et al.  Tinnitus impairs cognitive efficiency , 2004, International journal of audiology.

[47]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[48]  Timothy S. Coalson,et al.  A Surface-Based Analysis of Hemispheric Asymmetries and Folding of Cerebral Cortex in Term-Born Human Infants , 2010, The Journal of Neuroscience.

[49]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[50]  G. Andersson,et al.  Consequences of Suppressing Thoughts about Tinnitus and the Effects of Cognitive Distraction on Brain Activity in Tinnitus Patients , 2006, Audiology and Neurotology.

[51]  G. Andersson,et al.  Distinguishing levels of tinnitus distress. , 1999, Clinical otolaryngology and allied sciences.

[52]  Robert A. Levine,et al.  The auditory midbrain of people with tinnitus: Abnormal sound-evoked activity revisited , 2009, Hearing Research.

[53]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[54]  M. Mintun,et al.  The default mode network and self-referential processes in depression , 2009, Proceedings of the National Academy of Sciences.

[55]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[56]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[57]  P. van Dijk,et al.  Please Scroll down for Article Acta Oto-laryngologica Functional Imaging of Unilateral Tinnitus Using Fmri Functional Imaging of Unilateral Tinnitus Using Fmri , 2022 .

[58]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[60]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[61]  M. Greicius,et al.  Default-Mode Activity during a Passive Sensory Task: Uncoupled from Deactivation but Impacting Activation , 2004, Journal of Cognitive Neuroscience.

[62]  D. Bavelier,et al.  Cross-modal plasticity: where and how? , 2002, Nature Reviews Neuroscience.

[63]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[64]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[65]  Christian Gerloff,et al.  Dose‐dependent attenuation of auditory phantom perception (tinnitus) by PET‐guided repetitive transcranial magnetic stimulation , 2007, Human brain mapping.

[66]  Sachin Dixit,et al.  Functional connectivity for somatosensory and motor cortex in spastic diplegia , 2009, Somatosensory & motor research.

[67]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[68]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[69]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[70]  van Pim Dijk,et al.  Neural activity underlying tinnitus generation: Results from PET and fMRI , 2009, Hearing Research.

[71]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[72]  P. Wilson,et al.  Tinnitus reaction questionnaire: psychometric properties of a measure of distress associated with tinnitus. , 1991, Journal of speech and hearing research.

[73]  J. Eggermont,et al.  The neuroscience of tinnitus , 2004, Trends in Neurosciences.

[74]  Grant D Searchfield,et al.  Object identification and attention training for treating tinnitus. , 2007, Progress in brain research.

[75]  BMC Neuroscience , 2003 .

[76]  A. Norena,et al.  Reduced Attention Shift in Response to Auditory Changes in Subjects with Tinnitus , 2004, Audiology and Neurotology.

[77]  R A Levine,et al.  Lateralized tinnitus studied with functional magnetic resonance imaging: abnormal inferior colliculus activation. , 2000, Journal of neurophysiology.

[78]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[79]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.