Human Auditory and Adjacent Nonauditory Cerebral Cortices Are Hypermetabolic in Tinnitus as Measured by Functional Near-Infrared Spectroscopy (fNIRS)

Tinnitus is the phantom perception of sound in the absence of an acoustic stimulus. To date, the purported neural correlates of tinnitus from animal models have not been adequately characterized with translational technology in the human brain. The aim of the present study was to measure changes in oxy-hemoglobin concentration from regions of interest (ROI; auditory cortex) and non-ROI (adjacent nonauditory cortices) during auditory stimulation and silence in participants with subjective tinnitus appreciated equally in both ears and in nontinnitus controls using functional near-infrared spectroscopy (fNIRS). Control and tinnitus participants with normal/near-normal hearing were tested during a passive auditory task. Hemodynamic activity was monitored over ROI and non-ROI under episodic periods of auditory stimulation with 750 or 8000 Hz tones, broadband noise, and silence. During periods of silence, tinnitus participants maintained increased hemodynamic responses in ROI, while a significant deactivation was seen in controls. Interestingly, non-ROI activity was also increased in the tinnitus group as compared to controls during silence. The present results demonstrate that both auditory and select nonauditory cortices have elevated hemodynamic activity in participants with tinnitus in the absence of an external auditory stimulus, a finding that may reflect basic science neural correlates of tinnitus that ultimately contribute to phantom sound perception.

[1]  J J Eggermont,et al.  Spontaneous firing activity of cortical neurons in adult cats with reorganized tonotopic map following pure-tone trauma. , 2000, Acta oto-laryngologica.

[2]  David A. Boas,et al.  Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters , 2003, NeuroImage.

[3]  D. Ridder,et al.  Contralateral parahippocampal gamma-band activity determines noise-like tinnitus laterality: a region of interest analysis , 2011, Neuroscience.

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

[5]  J. Tian,et al.  Regional glucose metabolic increases in left auditory cortex in tinnitus patients: a preliminary study with positron emission tomography. , 2001, Chinese medical journal.

[6]  B. Pogue,et al.  Frequency-domain optical absorption spectroscopy of finite tissue volumes using diffusion theory. , 1994, Physics in medicine and biology.

[7]  J. Eggermont Cortical tonotopic map reorganization and its implications for treatment of tinnitus , 2006, Acta oto-laryngologica. Supplementum.

[8]  S. Arridge,et al.  Experimentally measured optical pathlengths for the adult head, calf and forearm and the head of the newborn infant as a function of inter optode spacing. , 1992, Advances in experimental medicine and biology.

[9]  D. Urbach,et al.  Auditory event related potentials in chronic tinnitus patients with noise induced hearing loss , 1993, Hearing Research.

[10]  Zhao Pengfei,et al.  Disrupted neural activity in unilateral vascular pulsatile tinnitus patients in the early stage of disease: Evidence from resting-state fMRI , 2015, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[11]  S R Arridge,et al.  Quantitation of pathlength in optical spectroscopy. , 1989, Advances in experimental medicine and biology.

[12]  J. Baizer,et al.  Understanding tinnitus: The dorsal cochlear nucleus, organization and plasticity , 2012, Brain Research.

[13]  Marco Ferrari,et al.  A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application , 2012, NeuroImage.

[14]  Matthias J. Wieser,et al.  Auditory cortex activation is modulated by emotion: A functional near-infrared spectroscopy (fNIRS) study , 2011, NeuroImage.

[15]  David A. Boas,et al.  A Quantitative Comparison of Simultaneous BOLD fMRI and NIRS Recordings during Functional Brain Activation , 2002, NeuroImage.

[16]  M. Ferrari,et al.  A brief review on the use of functional near-infrared spectroscopy (fNIRS) for language imaging studies in human newborns and adults , 2012, Brain and Language.

[17]  Dennis J. McFarland,et al.  Cutaneous-Evoked Tinnitus , 1999, Audiology and Neurotology.

[18]  Anders M. Dale,et al.  Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy , 2004, NeuroImage.

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

[20]  David A. Boas,et al.  A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans , 2006, NeuroImage.

[21]  S. Shore,et al.  Cross-modal interactions of auditory and somatic inputs in the brainstem and midbrain and their imbalance in tinnitus and deafness. , 2008, American journal of audiology.

[22]  L. M. Ward,et al.  Residual Inhibition Functions Overlap Tinnitus Spectra and the Region of Auditory Threshold Shift , 2008, Journal of the Association for Research in Otolaryngology.

[23]  J. J. Eggermont,et al.  Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus , 2003, Hearing Research.

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

[25]  S. Arridge,et al.  Estimation of optical pathlength through tissue from direct time of flight measurement , 1988 .

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

[27]  David A. Boas,et al.  A Systematic Comparison of Motion Artifact Correction Techniques for Functional Near-Infrared Spectroscopy , 2012, Front. Neurosci..

[28]  Leslie G. Ungerleider,et al.  Network analysis of cortical visual pathways mapped with PET , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  Abel,et al.  SPECT Imaging of Brain and Tinnitus-Neurotologic/Neurologic Implications. , 1995, The international tinnitus journal.

[30]  Paul Boersma,et al.  Praat, a system for doing phonetics by computer , 2002 .

[31]  S. Laureys,et al.  Connectivity graph analysis of the auditory resting state network in tinnitus , 2012, Brain Research.

[32]  Harold Burton,et al.  Altered networks in bothersome tinnitus: a functional connectivity study , 2012, BMC Neuroscience.

[33]  M Schwaiger,et al.  Focal metabolic activation in the predominant left auditory cortex in patients suffering from tinnitus: a PET study with [18F]deoxyglucose. , 1996, ORL; journal for oto-rhino-laryngology and its related specialties.

[34]  Ingrid S. Johnsrude,et al.  Functional Imaging of the Auditory System: The Use of Positron Emission Tomography , 2002, Audiology and Neurotology.

[35]  R. Coles,et al.  Epidemiology of tinnitus: (1) Prevalence , 1984, The Journal of Laryngology & Otology.

[36]  D. Delpy,et al.  Measurement of Cranial Optical Path Length as a Function of Age Using Phase Resolved Near Infrared Spectroscopy , 1994 .

[37]  Jinsheng Zhang,et al.  Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure , 2004, Neuroscience Letters.

[38]  A. Villringer,et al.  Beyond the Visible—Imaging the Human Brain with Light , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[39]  M. M. Richter,et al.  Cortical correlates of auditory sensory gating: A simultaneous near-infrared spectroscopy event-related potential study , 2009, Neuroscience.

[40]  R. Levine,et al.  Chapter 23 - Tinnitus , 2015 .

[41]  Berthold Langguth,et al.  The impact of auditory cortex activity on characterizing and treating patients with chronic tinnitus – first results from a PET study , 2006, Acta oto-laryngologica. Supplementum.

[42]  Dave R. M. Langers,et al.  Tonotopic mapping of human auditory cortex , 2014, Hearing Research.

[43]  H. Kojima,et al.  Active versus passive listening to auditory streaming stimuli: a near-infrared spectroscopy study. , 2010, Journal of biomedical optics.

[44]  D. Delpy,et al.  Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. , 1995, Physics in medicine and biology.

[45]  D. Boas,et al.  HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. , 2009, Applied optics.

[46]  Anne Schienle,et al.  Cortical activation during auditory elicitation of fear and disgust: A near-infrared spectroscopy (NIRS) study , 2013, Neuroscience Letters.

[47]  B. W. Murphy,et al.  The functional neuroanatomy of tinnitus , 1998, Neurology.

[48]  David A. Boas,et al.  Motion artifacts in functional near-infrared spectroscopy: A comparison of motion correction techniques applied to real cognitive data , 2014, NeuroImage.

[49]  D. De Ridder,et al.  The auditory and non-auditory brain areas involved in tinnitus. An emergent property of multiple parallel overlapping subnetworks , 2012, Front. Syst. Neurosci..

[50]  P. Adjamian The Application of Electro- and Magneto-Encephalography in Tinnitus Research – Methods and Interpretations , 2014, Front. Neurol..

[51]  Sana Amanat,et al.  TINNITUS , 1979, The Lancet.

[52]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[53]  R. Salvi,et al.  Evidence for limbic system links and neural plasticity , 1998 .

[54]  Chaozhe Zhu,et al.  Use of fNIRS to assess resting state functional connectivity , 2010, Journal of Neuroscience Methods.

[55]  Frank Mirz,et al.  Cortical Networks Subserving the Perception of Tinnitus - a PET Study , 2000, Acta oto-laryngologica. Supplementum.

[56]  David A. Boas,et al.  Quantification of the cortical contribution to the NIRS signal over the motor cortex using concurrent NIRS-fMRI measurements , 2012, NeuroImage.

[57]  Paul Boersma,et al.  Praat: doing phonetics by computer , 2003 .

[58]  P. Boersma Praat : doing phonetics by computer (version 5.1.05) , 2009 .

[59]  R. Zatorre,et al.  Human temporal-lobe response to vocal sounds. , 2002, Brain research. Cognitive brain research.

[60]  C. Newman,et al.  Auditory evoked cortical magnetic field (M100—M200) measurements in tinnitus and normal groups , 1991, Hearing Research.

[61]  M. Beauchamp,et al.  Auditory cortex activation to natural speech and simulated cochlear implant speech measured with functional near-infrared spectroscopy , 2014, Hearing Research.

[62]  Julian Keil,et al.  Mapping cortical hubs in tinnitus , 2009, BMC Biology.

[63]  Kathleen F Carlson,et al.  Hearing impairment and tinnitus: prevalence, risk factors, and outcomes in US service members and veterans deployed to the Iraq and Afghanistan wars. , 2015, Epidemiologic reviews.

[64]  G. Dumont,et al.  Wavelet based motion artifact removal for Functional Near Infrared Spectroscopy , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

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

[66]  M. Lauritzen,et al.  On the evidence of auditory evoked magnetic fields as an objective measure of tinnitus. , 1992, Electroencephalography and clinical neurophysiology.

[67]  Berthold Langguth,et al.  Functional Near-Infrared Spectroscopy to Probe State- and Trait-Like Conditions in Chronic Tinnitus: A Proof-of-Principle Study , 2014, Neural plasticity.

[68]  R. Parasuraman,et al.  Continuous monitoring of brain dynamics with functional near infrared spectroscopy as a tool for neuroergonomic research: empirical examples and a technological development , 2013, Front. Hum. Neurosci..