Tinnitus: maladaptive plasticity?
Abstract
Tinnitus is a symptom, not a disease. Tinnitus is often accompanied by hyperacusis as well as hearing loss. Tinnitus is foremost not an auditory disorder but a particular consequence of hearing loss, and then only in about 1/3 of the cases. Tinnitus can also result from insults such as whiplash, via somatic-auditory interaction in the dorsal cochlear nucleus. These are examples of bottom-up mechanisms that may underlie tinnitus. Much is known about necessary neural substrates of tinnitus, but much less about the sufficient ones. I will review proposals from animal research for these neural correlates, i.e., increased spontaneous firing rates, increased neural synchrony and reorganized cortical tonotopic maps. These can occur following noise trauma, but also following long-term exposure to non-traumatic (< 70 dBA) sounds. Homeostatic plasticity may play a role. I will compare these findings with what is known from human imaging and electrophysiology in tinnitus patients, and suggest that animal studies and human findings related to tinnitus are so far not fully compatible.References
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Eggermont, J.J., and Komiya, H. (2000). “Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood,” Hear. Res., 142, 89-101.
Eggermont, J.J., and Roberts, L.E. (2004). “The neuroscience of tinnitus,” Trends Neurosci., 27, 676-682.
Eggermont, J.J. (2013). “Hearing loss, hyperacusis, and tinnitus: what is modeled in animal research?” Hear. Res., 295, 140-149.
Gu, J.W., Halpin, C.F., Nam, E.C., Levine, R.A., and Melcher, J.R. (2010). “Tinnitus, diminished sound-level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity,” J. Neurophysiol., 104, 3361-3370.
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Jastreboff, P.J., and Hazell, J.W.P. (1993). “A neurophysiological approach to tinnitus: clinical implications,” Br. J. Audiol., 27, 7-17.
Kaltenbach, J.A., Zhang, J., and Afman, C.E. (2000). “Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure,” Hear. Res., 147, 282-292.
Kaltenbach, J.A., Zacharek, M.A., Zhang, J., and Frederick, S. (2004). “Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure,” Neurosci. Lett., 355, 121–125.
Knipper, M., Müller, M., and Zimmermann, U., (2012). “Molecular mechanisms of tinnitus,” in Tinnitus, Springer Handbook of Auditory Research 47. Edited by J.J. Eggermont, F.-G. Zeng, A.N. Popper, and R.R. Fay (Springer Science+Business Media, New York), pp. 59-82.
Kujawa, S.G., and Liberman, M.C. (2009). “Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss,” J. Neurosci., 29, 14077-14085.
Langers, D.M., de Kleine, E., and van Dijk, P. (2012). “Tinnitus does not require macroscopic tonotopic map reorganization,” Front. Syst. Neurosci., 6, 2.
Liberman, M.C., and Kiang, N.Y. (1978). “Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity,” Acta Oto-Laryngol. Suppl., 358, 1-63.
Makin, T.R., Scholz, J., Filippini, N., Slater, D.H., Tracey, I., and Johansen-Berg, H. (2013). “Phantom pain is associated with preserved structure and function in the former hand area,” Nat. Comm. 4, 1570.
Milbrandt, J.C., Holder, T.M., Wilson, M.C., Salvi, R.J., and Caspary, D.M. (2000). “GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma,” Hear. Res., 147, 251-260.
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Mulders, W.H., and Robertson, D. (2011). “Progressive centralization of midbrain hyperactivity after acoustic trauma,” Neurosci., 192, 753-760
Mulders, W.H.A.M., and Robertson, D. (2013). “Development of hyperactivity after acoustic trauma in the guinea pig inferior colliculus,” Hear. Res., 298, 104-108.
Munguia R, Pienkowski, M., and Eggermont, J.J. (2013). “Spontaneous firing rate changes in cat primary auditory cortex following long-term exposure to non traumatic noise. Tinnitus without hearing loss?” Neurosci. Lett., 546, 46-50.
Noreña, A., Micheyl, C., Chery-Croze, S., and Collet, L. (2002). “Psychoacoustic characterization of the tinnitus spectrum: implications for the underlying mechanisms of tinnitus,” Audiol. Neuro-Otol., 7, 358-369.
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Noreña, A.J., and Eggermont, J.J. (2005). “Enriched acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization,” J. Neurosci., 25, 699-705.
Noreña, A.J., and Eggermont, J.J. (2006). “Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus,” Neuroreport, 17, 559-563.
Rajan, R. (1998). “Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity,” Nat. Neurosci., 1, 138-143.
Rauschecker, J.P., Leaver, A.M., and Mühlau, M. (2010). “Tuning out the noise: limbic auditory interactions in tinnitus,” Neuron, 66, 819-826.
Roberts, L.E., Moffat, G., Baumann, M., Ward, L.M., and Bosnyak, D.J. (2008). “Residual inhibition functions overlap tinnitus spectra and the region of auditory threshold shift,” J. Assoc. Res. Oto., 9, 417-435.
Roberts, L.E., Eggermont, J.J., Caspary, D.M., Shore, S.E., Melcher, J.R., and Kaltenbach, J.A. (2010). “Ringing ears: the neuroscience of tinnitus,” J. Neurosci., 30, 14972–14979.
Roberts, L.E., Husain, F., and Eggermont, J.J. (2013) “Role of attention in the generation and modulation of tinnitus,” Neurosci. Biobehav. R., 37, 1754-1773.
Schaette, R., and Kempter, R. (2006). “Development of tinnitus-related neuronal hyperactivity through homeostatic plasticity after hearing loss: a computational model,” Eur. J. Neurosci., 23, 3124-3138.
Schaette, R., and Kempter, R. (2009). “Predicting tinnitus pitch from patients audiograms with a computational model for the development of neuronal hyperactivity,” J. Neurophysiol. 101, 3042-3052.
Seki, S., and Eggermont, J.J. (2002). “Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss,” Hear. Res., 173, 172-186.
Seki, S. and Eggermont, J.J. (2003). “Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss,” Hear. Res., 180, 28-38.
Turner, J.G., Hughes, L.F., and Caspary, D.M. (2005). “Divergent response properties of layer-V neurons in rat primary auditory cortex,” Hear. Res., 202, 129-140.
Turrigiano, G. (1999). “Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same,” Trends Neurosci., 22, 221-227.
Vogler, D.P., Robertson, D., and Mulders, W.H.A.M. (2011). “Hyperactivity in the ventral cochlear nucleus after cochlear trauma,” J. Neurosci., 31, 6639–6645.
Wang, H., Brozoski, T.J., Ling, L., Hughes, L.F., and Caspary, D.M. (2011). “Impact of sound exposure and aging on brain-derived neurotrophic factor and tyrosine kinase B receptors levels in dorsal cochlear nucleus 80 days following sound exposure,” Neurosci., 172, 453-459.
Wang, J., Ding, D., and Salvi, R.J. (2002). “Functional reorganization in chinchilla inferior colliculus associated with chronic and acute cochlear damage,” Hear. Res., 168, 238-249.
Ward, L.M. (2011). “The thalamic dynamic core theory of conscious experience,” Conscious. Cogn., 20, 464-486.
Weisz, N., Müller, S., Schlee, W., Dohrmann, K., Hartmann, T., and Elbert, T. (2007). “The neural code of auditory phantom perception,” J. Neurosci., 27, 1479-1484.
Yang, G., Lobarinas, E., Zhang, L., Turner, J., Stolzberg, D., Salvi, R., and Sun, W. (2007). “Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats,” Hear. Res., 226, 244-253.
Zacharek, M.A., Kaltenbach, J.A., Mathog, T.A., and Zhang, J. (2002) “Effects of co-chlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucle-us: implications for the origin of noise induced tinnitus,” Hear. Res., 172, 137-143.
Zhang, J.S., Kaltenbach, J.A., Godfrey, D.A., and Wang, J. (2006). “Origin of hyperactivity in the hamster dorsal cochlear nucleus following intense sound exposure,” J. Neurosci. Res., 84, 819-831.
Caspary, D.M., Schatteman, T.A., and Hughes, L.F. (2005). “Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs,” J. Neurosci., 25, 10952-10959.
Dauman, R., and Bouscau-Faure, F. (2005). “Assessment and amelioration of hyperacusis in tinnitus patients,” Acta Oto-Laryngol., 125, 503-509.
De Ridder, D., Elgoyhen, A.B., Romo, R., and Langguth, B. (2011). “Phantom percepts: Tinnitus and pain as persisting aversive memory networks,” Proc. Natl. Acad. Sci. USA, 108, 8075-8080.
Eggermont, J.J. (1992). “Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation and age,” J. Neurophysiol., 68, 1216-1228.
Eggermont, J.J., and Komiya, H. (2000). “Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood,” Hear. Res., 142, 89-101.
Eggermont, J.J., and Roberts, L.E. (2004). “The neuroscience of tinnitus,” Trends Neurosci., 27, 676-682.
Eggermont, J.J. (2013). “Hearing loss, hyperacusis, and tinnitus: what is modeled in animal research?” Hear. Res., 295, 140-149.
Gu, J.W., Halpin, C.F., Nam, E.C., Levine, R.A., and Melcher, J.R. (2010). “Tinnitus, diminished sound-level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity,” J. Neurophysiol., 104, 3361-3370.
Jastreboff, P.J. (1990). “Phantom auditory perception (tinnitus): mechanisms of generation and perception,” Neurosci. Res., 8, 228-251.
Jastreboff, P.J., and Hazell, J.W.P. (1993). “A neurophysiological approach to tinnitus: clinical implications,” Br. J. Audiol., 27, 7-17.
Kaltenbach, J.A., Zhang, J., and Afman, C.E. (2000). “Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure,” Hear. Res., 147, 282-292.
Kaltenbach, J.A., Zacharek, M.A., Zhang, J., and Frederick, S. (2004). “Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure,” Neurosci. Lett., 355, 121–125.
Knipper, M., Müller, M., and Zimmermann, U., (2012). “Molecular mechanisms of tinnitus,” in Tinnitus, Springer Handbook of Auditory Research 47. Edited by J.J. Eggermont, F.-G. Zeng, A.N. Popper, and R.R. Fay (Springer Science+Business Media, New York), pp. 59-82.
Kujawa, S.G., and Liberman, M.C. (2009). “Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss,” J. Neurosci., 29, 14077-14085.
Langers, D.M., de Kleine, E., and van Dijk, P. (2012). “Tinnitus does not require macroscopic tonotopic map reorganization,” Front. Syst. Neurosci., 6, 2.
Liberman, M.C., and Kiang, N.Y. (1978). “Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity,” Acta Oto-Laryngol. Suppl., 358, 1-63.
Makin, T.R., Scholz, J., Filippini, N., Slater, D.H., Tracey, I., and Johansen-Berg, H. (2013). “Phantom pain is associated with preserved structure and function in the former hand area,” Nat. Comm. 4, 1570.
Milbrandt, J.C., Holder, T.M., Wilson, M.C., Salvi, R.J., and Caspary, D.M. (2000). “GAD levels and muscimol binding in rat inferior colliculus following acoustic trauma,” Hear. Res., 147, 251-260.
Mulders, W.H. and Robertson, D. (2009). “Hyperactivity in the auditory midbrain after acoustic trauma: dependence on cochlear activity.” Neurosci., 164, 733-746.
Mulders, W.H., and Robertson, D. (2011). “Progressive centralization of midbrain hyperactivity after acoustic trauma,” Neurosci., 192, 753-760
Mulders, W.H.A.M., and Robertson, D. (2013). “Development of hyperactivity after acoustic trauma in the guinea pig inferior colliculus,” Hear. Res., 298, 104-108.
Munguia R, Pienkowski, M., and Eggermont, J.J. (2013). “Spontaneous firing rate changes in cat primary auditory cortex following long-term exposure to non traumatic noise. Tinnitus without hearing loss?” Neurosci. Lett., 546, 46-50.
Noreña, A., Micheyl, C., Chery-Croze, S., and Collet, L. (2002). “Psychoacoustic characterization of the tinnitus spectrum: implications for the underlying mechanisms of tinnitus,” Audiol. Neuro-Otol., 7, 358-369.
Noreña, A.J., and Eggermont, J.J. (2003). “Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus,” Hear. Res., 183, 137-153.
Noreña, A.J., and Eggermont, J.J. (2005). “Enriched acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization,” J. Neurosci., 25, 699-705.
Noreña, A.J., and Eggermont, J.J. (2006). “Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus,” Neuroreport, 17, 559-563.
Rajan, R. (1998). “Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity,” Nat. Neurosci., 1, 138-143.
Rauschecker, J.P., Leaver, A.M., and Mühlau, M. (2010). “Tuning out the noise: limbic auditory interactions in tinnitus,” Neuron, 66, 819-826.
Roberts, L.E., Moffat, G., Baumann, M., Ward, L.M., and Bosnyak, D.J. (2008). “Residual inhibition functions overlap tinnitus spectra and the region of auditory threshold shift,” J. Assoc. Res. Oto., 9, 417-435.
Roberts, L.E., Eggermont, J.J., Caspary, D.M., Shore, S.E., Melcher, J.R., and Kaltenbach, J.A. (2010). “Ringing ears: the neuroscience of tinnitus,” J. Neurosci., 30, 14972–14979.
Roberts, L.E., Husain, F., and Eggermont, J.J. (2013) “Role of attention in the generation and modulation of tinnitus,” Neurosci. Biobehav. R., 37, 1754-1773.
Schaette, R., and Kempter, R. (2006). “Development of tinnitus-related neuronal hyperactivity through homeostatic plasticity after hearing loss: a computational model,” Eur. J. Neurosci., 23, 3124-3138.
Schaette, R., and Kempter, R. (2009). “Predicting tinnitus pitch from patients audiograms with a computational model for the development of neuronal hyperactivity,” J. Neurophysiol. 101, 3042-3052.
Seki, S., and Eggermont, J.J. (2002). “Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss,” Hear. Res., 173, 172-186.
Seki, S. and Eggermont, J.J. (2003). “Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss,” Hear. Res., 180, 28-38.
Turner, J.G., Hughes, L.F., and Caspary, D.M. (2005). “Divergent response properties of layer-V neurons in rat primary auditory cortex,” Hear. Res., 202, 129-140.
Turrigiano, G. (1999). “Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same,” Trends Neurosci., 22, 221-227.
Vogler, D.P., Robertson, D., and Mulders, W.H.A.M. (2011). “Hyperactivity in the ventral cochlear nucleus after cochlear trauma,” J. Neurosci., 31, 6639–6645.
Wang, H., Brozoski, T.J., Ling, L., Hughes, L.F., and Caspary, D.M. (2011). “Impact of sound exposure and aging on brain-derived neurotrophic factor and tyrosine kinase B receptors levels in dorsal cochlear nucleus 80 days following sound exposure,” Neurosci., 172, 453-459.
Wang, J., Ding, D., and Salvi, R.J. (2002). “Functional reorganization in chinchilla inferior colliculus associated with chronic and acute cochlear damage,” Hear. Res., 168, 238-249.
Ward, L.M. (2011). “The thalamic dynamic core theory of conscious experience,” Conscious. Cogn., 20, 464-486.
Weisz, N., Müller, S., Schlee, W., Dohrmann, K., Hartmann, T., and Elbert, T. (2007). “The neural code of auditory phantom perception,” J. Neurosci., 27, 1479-1484.
Yang, G., Lobarinas, E., Zhang, L., Turner, J., Stolzberg, D., Salvi, R., and Sun, W. (2007). “Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats,” Hear. Res., 226, 244-253.
Zacharek, M.A., Kaltenbach, J.A., Mathog, T.A., and Zhang, J. (2002) “Effects of co-chlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucle-us: implications for the origin of noise induced tinnitus,” Hear. Res., 172, 137-143.
Zhang, J.S., Kaltenbach, J.A., Godfrey, D.A., and Wang, J. (2006). “Origin of hyperactivity in the hamster dorsal cochlear nucleus following intense sound exposure,” J. Neurosci. Res., 84, 819-831.
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2013-12-15
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Eggermont, J. J. (2013). Tinnitus: maladaptive plasticity?. Proceedings of the International Symposium on Auditory and Audiological Research, 4, 141–152. Retrieved from https://proceedings.isaar.eu/index.php/isaarproc/article/view/2013-15
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2013/3. Plasticity and auditory disorders
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