• 1990 (Vol.4)
  • 1989 (Vol.3)
  • 1988 (Vol.2)
  • 1987 (Vol.1)

Volume 32 #2

Contents

  1. Tinnitus – contemporary knowledge about its origin, electrophysiological correlates and treatment
  2. Eye optics and retinal topography in the nutria (Myocastor coypus)
  3. Quantitative study of Poggendorff illusion in school children with normal binocular vision and with strabismus
  4. The method of canine odor visualization
  5. Precopulatory mechanisms of reproductive isolation between two chromosomal forms of striped hamsters Cricetulus barabensis sensu lato (Rodentia, Cricetinae)
  6. Discrimination of sound signals with rippled spectra in on- and low-frequency noise: contribution of compressive nonlinearity and confounding issues
  7. The equivalent frequency-tuned filter form for discrimination of spectral pattern of sound signals: Contribution of the lateral suppression and harmonics

Tinnitus – contemporary knowledge about its origin, electrophysiological correlates and treatment

© 2018 N.G. Bibikov

JSC N.N. Andreyev Acoustical Institute 117036 Moscow, Shvernik st., 4

Received 10 Aug 2017

In this review we discuss contemporary literature that deals with problems of phantom sensation of sound (tinnitus). Various hypotheses concerning its origin, different physiological manifestations, as well as possible methods of treatment, are considered. We concentrated on the works dealing with the modeling of tinnitus on laboratory animals and on the studies of the role of peculiarities of auditory neurons impulse activity in this syndrome. Changes in the parameters of background firing in the dorsal cochlear nucleus and in the principal nucleus of the inferior colliculus are the most obvious correlates of this syndrome in laboratory animals. These changes are manifested in the increase in average frequency, in the enhancement of neuronal cross-correlation and in the appearance of burst activity. Results obtained in cortical structures, thalamus, and basal nuclei remain less clear. The most probable cause of tinnitus is a disturbance in the balance of excitation and inhibition in the process of plastic rearrangements of the auditory pathway. Physiological experiments in humans reveal a diversity of tinnitus genesis and its manifestations in cortical responses. We discuss plastic reorganization of receptive fields by prolonged presentation of specially selected stimuli as a promising method of treating tonal and narrowband tinnitus.

Key words: tinnitus, ringing in the ears, auditory neurons, spontaneous activity

DOI: 10.7868/S0235009218020014

Cite: Bibikov N. G. Tinnitus – sovremennye znaniya o ego proiskhozhdenii, elektrofiziologicheskikh korrelyatakh i o lechenii [Tinnitus – contemporary knowledge about its origin, electrophysiological correlates and treatment]. Sensornye sistemy [Sensory systems]. 2018. V. 32(2). P. 109-123 (in Russian). doi: 10.7868/S0235009218020014

References:

  • Adamchic I., Hauptmann C., Tass P.A. Changes of oscillatory activity in pitch processing network and related tinnitus: relief induced by acoustic CR neuromodulation. Frontier Syst. Neurosci. 2012. V. 6. Art. 18.
  • Adjamian P. The application of electro- and magnetoencephalography in tinnitus research – methods and interpretations. Frontier Neurol. 2014. V. 5. Art. 28.
  • Andersson G., Lyttkens L., Hirvelè C., Furmark T., Tillfors M., Fredrikson M. Regional cerebral bloodflow during tinnitus: a PET case study with lidocaine and auditory stimulation. Acta Otolaryngol. 2000. V. 120. P. 967–972.
  • Arnold W., Bar tenstein P., Oestreicher E.W.R., Schweiger M. Focal metabolic activation in the predominant left auditory cortex in patients suffering from tinnitus: a PET study with [18F]deoxyglucose. J. Oto-Rhino-Laryngol. 1996. V. 58. P. 195–199.
  • Ashton H., Reid K., Marsh R., Johnson I., Alter K., Griffiths T. High frequency localized ‘‘hot spots” in temporal lobes of patients with intractable tinnitus: a quantitative electroencephalographic (QEEG) study. Neurosci. Lett. 2007. V. 426. P. 23–28.
  • Baizer J.S., Manohar S., Paolone N.A., Weinstock N., Salvi R.J. Understanding tinnitus: the dorsal cochlear nucleus, organization and plasticity. Brain Res. 2012. V. 1485. P. 40–53.
  • Bauer C.A., Turner J.G., Caspary D.M., Myers K.S., Brozoski T.J. Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J. Neurosci. Res. 2008. V. 86. P. 2564–2578.
  • Bibikov N.G. Background firing in the auditory midbrain of the frog. IBRO Reports. 2017. V. 2. P. 54–62.
  • Bowen G.P., Lin D., Taylor M.K., Ison J.R. Auditory cortex lesions in the rat impair both temporal acuity and noise increment thresholds, revealing a common neural substrate. Cereb. Cortex. 2003. V. 13. P. 815–822.
  • Brozoski T.J., Bauer C.A., Caspary D.M. Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J. Neurosci. 2002. V. 22. P. 2383–2390.
  • Brozoski T.J., Bauer C.A. The effect of dorsal cochlear nucleus ablation on tinnitus in rats. Hear. Res. 2005. V. 206. P. 227–236.
  • Brozoski T.J., Wisner K.W., Sybert L.T., Bauer C.A. Bilateral dorsal cochlear nucleus lesions prevent acoustic-trauma induced tinnitus in an animal model. J. Assoc. Res. Otolaryngol. 2012. V. 3. P. 55–66.
  • Darlington C.L., Smith P.F. Drug treatments for tinnitus. Prog. Brain Res. 2007. V. 166. P. 249–262.
  • Davies J.E., Gander P., Hall D.A. Does chronic tinnitus alter the emotional response function of the amygdala?: a sound-evoked FMRI study. Frontier Aging Neurosci. 2017. V. 9. Art. 31.
  • Dong S., Rodger J., Mulders W.H., Robertson D. Tonotopic changes in GABA receptor expression in guinea pig inferior colliculus after partial unilateral hearing loss. Brain research. 2010. V. 1342. P. 24–32.
  • Du X., Chen K., Choi C.H., Li W., Cheng W., Stewart C., Hu N., Floyd R.A., Kopke R.D. Selective degeneration of synapses in the dorsal cochlear nucleus of chinchilla following acoustic trauma and effects of antioxidant treatment. Hear. Res. 2012. V. 283. P. 1–13.
  • Eggermont J.J. Firing rate and firing synchrony distinguish dynamic from steady state sound. Neuroreport. 1997. V. 8. P. 2709–2713.
  • Eggermont J.J. Hearing loss, hyperacusis, or tinnitus: What is modeled in animal research? Hear. Res. 2013. V. 295. P. 140–149.
  • Eggermon J.J., Roberts L.E. The neuroscience of tinnitus. Trends Neurosci. 2004. V. 27. P. 676–682.
  • Eggermont J.J., Tass P.A. Maladaptive neural synchrony in tinnitus: origin and restoration. Frontier Neurol. 2015. V. 6. Art. 29.
  • Elgoyhen A.B., Langguth B., De Ridder D., Vanneste S. Tinnitus: perspective from human neuroimaging. Nat. Rev. Neurosci. 2015. V. 16(10). P. 632–642.
  • Engineer N.D., Møller A.R., Kilgard M.P. Directing neural plasticity to understand and treat tinnitus. Hear. Res. 2013. V. 295. P. 58–66.
  • Finlayson P.G., Kaltenbach J.A. Alterations in the spontaneous discharge patterns of single units in the dorsal cochlear nucleus following intense sound. Hear.Res. 2009. V. 256. P. 104–117.
  • Galazyuk A.V., Voytenk S.V., Longenecker R.J. Long-lasting forward suppression of spontaneous firing in auditory neurons: implication to the residual inhibition of tinnitus. J. Assoc. Res. Otolaryngol. 2017. V. 18(2). P. 343–353.
  • Gao Y., Manzoor N., Kaltenbach J.A. Evidence of activitydependent plasticity in the dorsal cochlear nucleus, in vivo, induced by brief sound exposure. Hear. Res. 2016. V. 341. P. 31–42.
  • Grigor’ev D.Y., Bibikov N.G. Model of a neuron trained to extract periodicity. Acoustical Physics. 2010. V. 56(5). P. 720–728.
  • Gu J.W., Herrmann B.S., Levine R.A., Melcher J.R. Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus. J. Assoc. Res. Otolaryngol. 2012. V. 13. P. 819–833.
  • Guitton M.J., Caston J., Ruel J., Johnson R.M., Pujol R., Puel J.L. Salicylate induces tinnitus through activation of cochlear NMDA receptors. J. Neurosci. 2003. V. 23. P. 3944–3952.
  • Hebert S., Fournier P., Noreña A. The auditory sensitivity is increased in tinnitus ears. J. Neurosci. 2013. V. 33. P. 2356–2364.
  • Heller M.F., Bergman M. Tinnitus aurium in normally hearing persons. Ann. Otol. Rhinol. Laryngol. 1953. V. 62. P. 73–83.
  • Hesse L.L., Bakay W., Ong H.-C., Anderson L., Ashmore J., McAlpine D., Linden J., Schaette R. Non-monotonic relation between noise exposure severity and neuronal hyperactivity in the auditory midbrain. Frontier Neurol. 2016. V. 7. Art. 133.
  • Imig T.J., Bibikov N.G., Pourrier P., Samson F.K. Directionality derived from pinna-cue spectral notches in cat dorsal cochlear nucleus. J. Neurophysiol. 2000. V. 83. P. 907–925.
  • Imig T.J., Durham D. Effect of unilateral noise exposure on the tonotopic distribution of spontaneous activity in the cochlear nucleus and inferior colliculus in the cortically intact and decorticate rat. J. Comp. Neurol. 2005. V. 490. P. 391–413.
  • Jastreboff P.J., Brennan J.F., Sasaki C.T. An animal model for tinnitus. Laryngoscope. 1988. V. 98. P. 280–286.
  • Jeanmonod D., Magnin M., Morel A. Low-threshold calcium spike bursts in the human thalamus. Brain. 1996. V. 119. P. 363–375.
  • Kalcioglu M.T., Bayindir T., Erdem T., Ozturan O. Objective evaluation of the effects of intravenous lidocaine on tinnitus. Hear. Res. 2005. V. 199. P. 81–88.
  • Kaltenbach J.A. The dorsal cochlear nucleus as a participant in the auditory, attentional nd emotional components of tinnitus. Hear. Res. 2006. V. 216–217. P. 224–234.
  • Kaltenbach J.A., Afman C.E. Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone evoked activity: a physiological model for tinnitus. Hear. Res. 2000. V. 140. P. 165–172.
  • Kaltenbach J.A., Zacharek M.A., Zhang J., Frederick S. Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure. Neurosci. Lett. 2004. V. 355. P. 121–125.
  • Koehler S.D., Shore S.E. Stimulus timing-dependent plasticity in dorsal cochlear nucleus is altered in tinnitus. J. Neurosci. 2013. V. 33(50):19647–19656.
  • König O., Schaette R., Kempter R., Gross M. Course of hearing loss and occurrence of tinnitus. Hear. Res. 2006. V. 221. P. 59–64.
  • Krauss P., Hoppe U., Schulze H. Stochastic resonance controlled upregulation of internal noise after hearing loss as a putative cause of tinnitus-related neuronal hyperactivity. Frontier Neuroscie. 2016. V. 10. Art. 597.
  • Lanting C.P., Kleine E., van Dijk P. Neural activity underlying tinnitus generation: Results from PET and fMRI. Hear. Res. 2009. V. 255. P. 1–13.
  • Lewis J.E., Stephens S.D., McKenna L. Tinnitus and suicide. Clin.Otolaryngol.Allied Sci. 1994. V. 19. P. 50–54.
  • Liberman M.C., Dodds L.W. Single-neuron labeling and chronic cochlear pathology: part II. Stereocilia damage and alterations of spontaneous discharge rates. Hear. Res. 1984. V. 16. P. 43–53.
  • Liberman L.D., Liberman M.C. Dynamics of cochlear synaptopathy after acoustic overexposure. J. Assoc. Res. Otolaryngol. 2015. V. 16. P. 205–219.
  • Lobarinas E., Sun W., Cushing R., Salvi R. A novel behavioral paradigm for assessing tinnitus using scheduleinduced polydipsia avoidance conditioning (SIP-AC). Hear. Res. 2004. V. 190. P. 109–114.
  • Lobarinas E., Hayes S.H., Allman B.L. The gap-startle paradigm for tinnitus screening in animal models: limitations and optimization. Hear. Res. 2013. V. 295. P. 150–160.
  • Lockwood A.H., Salvi R.J., Coad M.L., Towsley M.L., Wack D.S., Murphy B.W. The functional neuroanatomy of tinnitus: evidence for limbic system links and neural plasticity. Neurology. 1998. V. 50. P. 114–120.
  • Lockwood A.H., Wack D.S., Burkard R.F., Coad M.L., Reyes S.A., Arnold S.A., Salvi R.J. The functional anatomy of gaze-evoked tinnitus and sustained lateral gaze. J. Neurology. 2001. V. 56. P. 472–480.
  • Longenecker R.J., Galazyuk A.V. Development of tinnitus in CBA/CaJ mice following sound exposure. J. Assoc. Res. Otolaryngol. 2011. V. 12. P. 647–658.
  • Lorenz I., Müller N., Schlee W., Har tmann T., Weisz N. Loss of alpha power is related to increased gamma synchronization-A marker of reduced inhibition in tinnitus? Neurosci. Lett. 2009. V. 453(3). P. 225–228.
  • Lorenz I., Müller N., Schlee W., Langguth B., Weisz N. Short-term effects of single repetitive TMS sessions on auditory evoked activity in patients with chronic tinnitus. J. Neurophysiol. 2010. V. 104. P. 1497–1505.
  • Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001. V. 412. P. 150–157.
  • Londero A., Llummis R.C., Guttman N. Exploratory studies of Zwicker’s “negative afterimage” in hearing. J. Acoust. Soc. Am. 1972. V. 51. P. 1930–1944.
  • Ma W.L., Young E.D. Dorsal cochlear nucleus response properties following acoustic trauma: response maps and spontaneous activity. Hear. Res. 2006. V. 216–217. P. 176–188.
  • Mahlke C., Wallhausser-Franke E. Evidence for tinnitusrelated plasticity in the auditory and limbic system, demonstrated by arg3.1 and c-fos immunocytochemistry. Hear. Res. 2004. V. 195. P. 17–34.
  • Manzoor N.F., Licari F., Klapchar M., Elkin R.L., Gao Y., Chen G., Kaltenbach J.A. Noise-induced hyperactivity in the inferior colliculus: its relationship with hyperactivity in the dorsal cochlear nucleus. J. Neurophysiol. 2012. V. 108. P. 976–988.
  • Masterton R.B., Granger E.M., Glendenning K.K. Role of acoustic striae in hearing: mechanism for enhancement of sound detection in cats. Hear Res. 1994. V. 73(2). P. 209–222.
  • Møller A. Tinnitus: presence and future. Prog. Brain. Res. 2007. V. 166. P. 3–16.
  • Marsat G., Pollack G.S. A behavioral role for feature detection by sensory bursts. J. Neuroscie. 2006. V. 26(41). P. 10542–10547.
  • Mulders W.H., Robertson D. Hyperactivity in the auditory midbrain after acoustic trauma: dependence on cochlear activity. Neuroscience. 2009. V. 164. P. 733–746.
  • Mulders W.H., Robertson D. Development of hyperactivity after acoustic trauma in the guinea pig inferior colliculus. Hear. Res. 2013. V. 298. P. 104–108.
  • Mulders W.H., Spencer T.C., Robertson D. Effects of pulsatile electrical stimulation of the round window on central hyperactivity after cochlear trauma in guinea pig. Hear. Res. 2016. V. 335. P. 128–137.
  • Neff P., Michels J., Meyer M., Schecklmann M., Langguth B., Schlee W. 10 Hz amplitude modulated sounds induce short-term tinnitus suppression. Frontier Aging Neurosci. 2017. V. 9. Art.130.
  • Parra L.C., Pearlmutter B.A. Illusory percepts from auditory adaptation. J. Acoust. Soc. Am. 2007. V. 121(3). P. 1632–1641.
  • Pilati N., Large C., Forsythe I.D., Hamann M. Acoustic overexposure triggers burst firing in dorsal cochlear nucleus fusiform cells. Hear. Res. 2012. V. 283. P. 98–106.
  • Plewnia C., Reimold M., Najib A., Brehm B., Reischl G., Plontke S.K., Gerloff C. Dose-dependent attenuation of auditory phantom perception (tinnitus) by PET-guided repetitive transcranial magnetic stimulation. Hum. Brain Mapp. 2007. V. 28. P. 238–246.
  • Popovych O.V., Xenakis M.N., Tass P.A. The spacing principle for unlearning abnormal neuronal synchrony. PLoS One. 2015. V. 10(2): e0117205.
  • Pridmore S., Kleinjung T., Langguth B., Eichhammer P. Transcranial magnetic stimulation: potential treatment for tinnitus? Psychiatry Clin.Neurosci. 2006. V. 60. P. 133–138.
  • Rubinstein J.T., Tyler R.S., Johnson A., Brown C.J. Electrical suppression of tinnitus with high-rate pulse trains. Otol. Neurotol. 2003. V. 24. P. 478–485.
  • Roberts L.E., Eggermont J.J., Caspary D.M., Shore S.E., Melcher J.R., Kaltenbach J.A. Ringing ears: the neuroscience of tinnitus. J. Neurosci. 2010. V. 30(45). P. 14972–14979.
  • Schaette R., König O., Hornig D., Gross M., Kempter R. Acoustic stimulation treatments against tinnitus could be most effective when tinnitus pitch is within the stimulated frequency range. Hear. Res. 2010. V. 269. P. 95–101.
  • Schaette R., McAlpine D. Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J. Neurosci. 2011. V. 31. P. 13452–13457.
  • Schaette R., Turtle C., Munro K.J. Reversible induction of phantom auditory sensations through simulated unilateral hearing loss. PLoS One. 2012. V. 7: e35238.
  • Schneider P., Andermann M., Wengenroth M., Goebel R., Flor H., Rupp A., Diesch E. Reduced volume of Heschl’s gyrus in tinnitus. Neuroimage. 2009. V. 45 (3). P. 927–939.
  • Seki S., Eggermont J.J. Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear. Res. 2003. V. 180. P. 28–38.
  • Shore S. Somatosensory projections to cochlear nucleus are upregulated after unilateral deafness. J. Neurosci. 2012. V. 32. P. 15791–15801.
  • Shore S., Zhou J., Koehler S. Neural mechanisms underlying somatic tinnitus. Prog Brain Res. 2007. V. 166. P. 107–123.
  • Singla S., Dempsey C., Warren R., Enikolopov A.G., Sawtel N.B. A cerebellum-like circuit in the auditory system cancels responses to self-generated sound. Nature Neuroscience. 2017. V. 20(7). P. 943–950.
  • Szczepaniak W.S., Møller A.R. Effects of baclofen, clonazepam, and diazepam on tone exposure induced hyperexcitability of the inferior colliculus in the rat: possible therapeutic implications for pharmacological management of tinnitus and hyperacusis. Hear. Res. 1996. V. 97. P. 46–53.
  • Tass P.A. Desynchronization of brain rhythms with soft phase-resetting techniques. Biol. Cybern. 2002. V. 87. P. 102–115.
  • Tass P.A., Adamchic I., Freund H.-J., von Stackelberg T., Hauptmann C. Counteracting tinnitus by acoustic coordinated reset neuromodulation. Restor. Neurol. Neurosci. 2012. V. 30. P. 137–159.
  • Theodoroff S.M., Folmer R.L. Repetitive transcranial magnetic stimulation as a treatment for chronic tinnitus: a critical review. Otol. Neurotol. 2013. V. 34(2). P. 199–208.
  • Turner J.G., Brozoski T.J., Bauer C.A., Parrish J.L., Myers K., Hughes L.F., Caspary D.M. Gap detection deficits in rats with tinnitus: a potential novel screening tool. Behav. Neurosci. 2006. V. 120. P. 188–195.
  • Tziridis K., Ahlf S., Jeschke M., Happel M.F.K., Ohl F.W., Schulze H. Noise trauma induced neural plasticity throughout the auditory system of Mongolian gerbils: differences between tinnitus developing and nondeveloping animals. Frontier Neurol. 2015. V. 6. Art. 22.
  • Vaness S., de Rider D. Bifrontal transcranial direct current stimulation modulates tinnitus intensity and tinnitusdistress-related brain activity. Europ. J. Neurosci. 2011. V. 34. P. 605–614.
  • Vogler D.P., Robertson D., Mulders W.H. Hyperactivity in the ventral cochlear nucleus after cochlear trauma. J. Neurosci. 2011. V. 31(18). P. 6639–6645.
  • Vogler D.P., Robertson D., Mulders W.H. Influence of the paraflocculus on normal and abnormal spontaneous firingrates in the inferior colliculus. Hear. Res. 2016. V. 333. P. 1–7.
  • Weinberger N.M. Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. Learn. Mem. 2007. V. 14. P. 1–16.
  • Weisz N., Wienbruch C., Dohrmann K., Elbert T. Neuromagnetic indicators of auditory cortical reorganization of tinnitus. Brain. 2005. V. 128. P. 2722–2731
  • Weisz N., Muller S., Schlee W., Dohrmann K., Hartmann T., Elbert T. The neural code of auditory phantom perception. J. Neurosci. 2007. V. 27. P. 1479–1484.
  • Westerberg B.D., Roberson J.B., Stach B.A. A double-blind placebo-controlled trial of baclofen in the treatment of tinnitus. Am. J. Otol. 1996. V. 17. P. 896–903.
  • Wilson J.P. Evidence for a cochlear origin for acoustic reemissions, threshold fine-structure and tonal tinnitus. Hear. Res. 1980. V. 2(3,4). P. 233–252.
  • Wu C., Martel D.T., Shore S.E. Increased synchrony and bursting of dorsal cochlear nucleus fusiform cells correlate with tinnitus. J. Neurosci. 2016. V. 36(6). P. 2068–2073.
  • Xiong B., Alkharabsheh A., Manohar S., Chen G., Yu N., Zhao X., Salvi R., Sun W. Hyperexcitability of inferior colliculus and acoustic startle reflex with age-related hearing loss. Hear. Res. 2017. V. 350. P. 32–42.
  • Yang G., Lobarinas E., Zhang L., Turner J., Stolzberg D., Salvi R., Sun W. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awakerats. Hear. Res. 2007. V. 226. P. 244–253.
  • Zacharek M.A., Kaltenbach J.A., Mathog T.A., Zhang J. Effects of cochlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucleus: implications for the origin of noise induced tinnitus. Hear. Res. 2002. V. 172. P. 137–144.
  • Zeng F.G., Tang Q., Dimitrijevic A., Starr A., Larky J., Blevins N.H. Tinnitus suppression by low-rate electric stimulation and its electrophysiological mechanisms. Hear. Res. 2011. V. 277. P. 61–66.
  • Zhang J.S., Kaltenbach J.A., Godfrey D.A., Wang J. Origin of hyperactivity in the hamster dorsal cochlear nucleus following intense sound exposure. J. Neurosci. Res. 2006. V. 84. P. 819–831.
  • Zhang X., Yang P., Cao Y., Qin L., Sato Y. Salicylate induced neural changes in the primary auditory cortex of awake cats. Neuroscience. 2011. V. 172. P. 232–245.
  • Zugaib J., Ceballos C.C., Leao R.M. High doses of salicylate reduces glycinergic inhibition in the dorsal cochlear nucleus of the rat. Hear. Res. 2016. V. 332. P. 188–198.
  • Zwicker E. “Negative afterimage” in hearing. J. Acoust. Soc. Am. 1964. V. 36. P. 2413–2415.