Dorsal cochlear nucleus hyperactivity and tinnitus: are they related?

PURPOSE Eight lines of evidence implicating the dorsal cochlear nucleus (DCN) as a tinnitus contributing site are reviewed. We now expand the presentation of this model, elaborate on its essential details, and provide answers to commonly asked questions regarding its validity. CONCLUSIONS Over the past decade, numerous studies have converged to support the hypothesis that the DCN may be an important brain center in the generation and modulation of tinnitus. Although other auditory centers have been similarly implicated, the DCN deserves special emphasis because, as a primary acoustic nucleus, it occupies a potentially pivotal position in the hierarchy of functional processes leading to the emergence of tinnitus percepts. Moreover, because a great deal is known about the underlying cellular categories and the details of synaptic circuitry within the DCN, this brain center offers a potentially powerful model for probing mechanisms underlying tinnitus.

[1]  R. Bilger,et al.  Consistent within-session measures of tinnitus. , 1992, Journal of speech and hearing research.

[2]  Pawel J. Jastreboff,et al.  Salicylate-induced abnormal activity in the inferior colliculus of rats , 1995, Hearing Research.

[3]  J. Janisse,et al.  Increases in spontaneous neural activity in the hamster dorsal cochlear nucleus following cisplatin treatment: a possible basis for cisplatin-induced tinnitus , 2002, Hearing Research.

[4]  D. A. Godfrey,et al.  Effects of parallel fiber stimulation on neurons of rat dorsal cochlear nucleus , 1996, Hearing Research.

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

[6]  R. Kempter,et al.  Development of hyperactivity after hearing loss in a computational model of the dorsal cochlear nucleus depends on neuron response type , 2008, Hearing Research.

[7]  W. D. Winters,et al.  Multiple unit activity of dorsal cochlear nucleus and midbrain reticular formation during paradoxical phase of sleep. IV, A supplementary note. , 1972, Electroencephalography and clinical neurophysiology.

[8]  Raphael Lorente De No,et al.  The Primary Acoustic Nuclei , 1981 .

[9]  D. A. Godfrey,et al.  Comparison of γ-aminobutyrate receptors in the medial vestibular nucleus of control and Scn8a mutant mice , 2007, Brain Research.

[10]  R S Tyler,et al.  The determination of tinnitus loudness considering the effects of recruitment. , 1983, Journal of speech and hearing research.

[11]  R. Salvi,et al.  Tinnitus and neural activity. , 1983, Journal of speech and hearing research.

[12]  S. Shore,et al.  Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation , 2005, The European journal of neuroscience.

[13]  D. Ryugo,et al.  Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat , 1996, The Journal of comparative neurology.

[14]  C. G. Benson,et al.  Altered glycinergic synaptic activities in guinea pig brain stem auditory nuclei after unilateral cochlear ablation , 2000, Hearing Research.

[15]  D. A. Godfrey,et al.  Effects of cochlear ablation on muscarinic acetylcholine receptor binding in the rat cochlear nucleus , 2006, Journal of neuroscience research.

[16]  James A. Kaltenbach,et al.  Chemistry of Granular and Closely Related Regions of the Cochlear Nucleus , 1997 .

[17]  K. Osen,et al.  Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. , 1984, Archives italiennes de biologie.

[18]  Khalid Hamasha,et al.  Otoacoustic Emissions and Tinnitus in Normal Hearing , 2010 .

[19]  J. Kaltenbach The dorsal cochlear nucleus as a contributor to tinnitus: mechanisms underlying the induction of hyperactivity. , 2007, Progress in brain research.

[20]  D. A. Godfrey,et al.  Effects of intense tone exposure on choline acetyltransferase activity in the hamster cochlear nucleus , 2006, Hearing Research.

[21]  G. Chermak,et al.  Characteristics of temporary noise-induced tinnitus in male and female subjects. , 1987, Scandinavian audiology.

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

[23]  Jinsheng Zhang,et al.  Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound , 1998, Neuroscience Letters.

[24]  Z Vass,et al.  Trigeminal ganglion innervates the auditory brainstem , 2000, The Journal of comparative neurology.

[25]  E. M. Burns A comparison of variability among measurements of subjective tinnitus and objective stimuli. , 1984, Audiology : official organ of the International Society of Audiology.

[26]  D. K. Morest,et al.  Neuronal and transneuronal degeneration of auditory axons in the brainstem after cochlear lesions in the chinchilla: cochleotopic and non-cochleotopic patterns , 1997, Hearing Research.

[27]  A. Møller,et al.  Some forms of tinnitus may involve the extralemniscal auditory pathway , 1992, The Laryngoscope.

[28]  C. Sekirnjak,et al.  Long-Lasting Increases in Intrinsic Excitability Triggered by Inhibition , 2003, Neuron.

[29]  P. Finlayson,et al.  Alterations in the spontaneous discharge patterns of single units in the dorsal cochlear nucleus following intense sound exposure , 2009, Hearing Research.

[30]  J. Kaltenbach,et al.  Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone-evoked activity: a physiological model for tinnitus , 2000, Hearing Research.

[31]  R. McCrea,et al.  Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo‐ocular reflexes of the squirrel monkey , 1987, The Journal of comparative neurology.

[32]  A. Axelsson,et al.  Tinnitus in noise-induced hearing loss. , 1985, British journal of audiology.

[33]  Jinsheng Zhang,et al.  Effects of cochlear ablation on noise induced hyperactivity in the hamster dorsal cochlear nucleus: implications for the origin of noise induced tinnitus , 2002, Hearing Research.

[34]  C. G. Benson,et al.  Plastic Changes in Glycine and GABA Release and Uptake in Adult Brain Stem Auditory Nuclei after Unilateral Middle Ear Ossicle Removal and Cochlear Ablation , 1998, Experimental Neurology.

[35]  K. Osen Course and termination of the primary afferents in the cochlear nuclei of the cat. An experimental anatomical study. , 1970, Archives italiennes de biologie.

[36]  D. A. Godfrey,et al.  Effects of acoustic trauma on dorsal cochlear nucleus neuron activity in slices , 2002, Hearing Research.

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

[38]  R. Weinberg,et al.  A cuneocochlear pathway in the rat , 1987, Neuroscience.

[39]  D. A. Godfrey,et al.  Changes in spontaneous neural activity in the dorsal cochlear nucleus following exposure to intense sound: relation to threshold shift , 1998, Hearing Research.

[40]  C Helmchen,et al.  Diverse effects of Purkinje cell loss on deep cerebellar and vestibular nuclei neurons in Purkinje cell degeneration mutant mice: A possible compensatory mechanism , 1997, The Journal of comparative neurology.

[41]  R. Petralia,et al.  Differential distribution of glutamate receptors in the cochlear nuclei , 2000, Hearing Research.

[42]  R. Levine,et al.  CNS somatosensory-auditory interactions elicit or modulate tinnitus , 2003, Experimental Brain Research.

[43]  D. A. Godfrey,et al.  Effects of trapezoid body and superior olive lesions on choline acetyltransferase activity in the rat cochlear nucleus , 1987, Hearing Research.

[44]  Alberti Pw Tinnitus in occupational hearing loss: nosological aspects. , 1987 .

[45]  M. J. Penner Variability in matches to subjective tinnitus. , 1983, Journal of speech and hearing research.

[46]  D. McFarland,et al.  Anomalous cross-modal plasticity following posterior fossa surgery: Some speculations on gaze-evoked tinnitus , 1994, Hearing Research.

[47]  J. Helms,et al.  The High Rate CIS Auditory Brainstem Implant for Restoration of Hearing in NF-2 Patients. , 2007, Skull base : official journal of North American Skull Base Society ... [et al.].

[48]  S. Zhang,et al.  Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. , 1993, Journal of neurophysiology.

[49]  Auditory perceptual and visual-spatial characteristics of gaze-evoked tinnitus. , 1994, Audiology : official organ of the International Society of Audiology.

[50]  H. Heffner,et al.  Tinnitus in hamsters following exposure to intense sound , 2002, Hearing Research.

[51]  G. M. Gerken,et al.  Hypersensitivity to electrical stimulation of auditory nuclei follows hearing loss in cats , 1984, Hearing Research.

[52]  M. Loeb,et al.  Relation of induced tinnitus to physical characteristics of the inducing stimuli. , 1966, The Journal of the Acoustical Society of America.

[53]  T. Brozoski,et al.  The effect of dorsal cochlear nucleus ablation on tinnitus in rats , 2005, Hearing Research.

[54]  Matthew Lewandowski,et al.  Cisplatin-induced hyperactivity in the dorsal cochlear nucleus and its relation to outer hair cell loss: relevance to tinnitus. , 2002, Journal of neurophysiology.

[55]  T. Tzounopoulos Mechanisms of synaptic plasticity in the dorsal cochlear nucleus: plasticity-induced changes that could underlie tinnitus. , 2008, American journal of audiology.

[56]  Jianxun Zhou,et al.  Projections from the trigeminal nuclear complex to the cochlear nuclei: A retrograde and anterograde tracing study in the guinea pig , 2004, Journal of neuroscience research.

[57]  A. Cacace,et al.  Expanding the biological basis of tinnitus: crossmodal origins and the role of neuroplasticity , 2003, Hearing Research.

[58]  C. Haenggeli,et al.  Multimodal inputs to the granule cell domain of the cochlear nucleus , 2003, Experimental Brain Research.

[59]  T. Imig,et al.  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 , 2005, The Journal of comparative neurology.

[60]  L F Hughes,et al.  Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise‐induced hearing loss , 2007, The European journal of neuroscience.

[61]  Loudness adaptation and excitation patterns: effects of frequency and level. , 1997, The Journal of the Acoustical Society of America.

[62]  D. Caspary,et al.  Elevated Fusiform Cell Activity in the Dorsal Cochlear Nucleus of Chinchillas with Psychophysical Evidence of Tinnitus , 2002, The Journal of Neuroscience.

[63]  R. Levine,et al.  Muscle Contractions and Auditory Perception in Tinnitus Patients and Nonclinical Subjects , 2004, Cranio : the journal of craniomandibular practice.

[64]  G. Spirou,et al.  Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus , 1994, The Journal of comparative neurology.

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

[66]  Lionel Collet,et al.  Psychoacoustic Characterization of the Tinnitus Spectrum: Implications for the Underlying Mechanisms of Tinnitus , 2002, Audiology and Neurotology.

[67]  R. Tyler,et al.  Masking of tinnitus compared to masking of pure tones. , 1984, Journal of speech and hearing research.

[68]  J. Kaltenbach,et al.  Tonotopic maps obtained from the surface of the dorsal cochlear nucleus of the hamster and rat , 1991, Hearing Research.

[69]  James A. Kaltenbach,et al.  Tinnitus as a plastic phenomenon and its possible neural underpinnings in the dorsal cochlear nucleus , 2005, Hearing Research.

[70]  R. Altschuler,et al.  Deafness‐related decreases in glycine‐immunoreactive labeling in the rat cochlear nucleus , 2005, Journal of neuroscience research.

[71]  D. A. Godfrey,et al.  Glutamatergic transmission of neuronal responses to carbachol in rat dorsal cochlear nucleus slices , 1999, Neuroscience.

[72]  E D Young,et al.  Proprioceptive Information from the Pinna Provides Somatosensory Input to Cat Dorsal Cochlear Nucleus , 2001, The Journal of Neuroscience.

[73]  M. Charles Liberman,et al.  Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates , 1984, Hearing Research.

[74]  J. Tonndorf The analogy between tinnitus and pain: A suggestion for a physiological basis of chronic tinnitus , 1987, Hearing Research.

[75]  J. Kaltenbach Summary of evidence pointing to a role of the dorsal cochlear nucleus in the etiology of tinnitus , 2006, Acta oto-laryngologica. Supplementum.

[76]  M. Rosenberg,et al.  Gaze‐evoked tinnitus , 1987, Neurology.

[77]  Cisplatin-induced Increases in Spontaneous Neural Activity in the Dorsal Cochlear Nucleus and Associated Outer Hair Cell Loss , 2000, Audiology : official organ of the International Society of Audiology.

[78]  Investigation of tinnitus induced by sound and its relationship to ongoing tinnitus. , 1989, Journal of speech and hearing research.

[79]  Wilson Jp Otoacoustic emissions and tinnitus. , 1986 .

[80]  D. McCaslin,et al.  Increases in Spontaneous Activity in the Dorsal Cochlear Nucleus Following Exposure to High Intensity Sound: A Possible Neural Correlate of Tinnitus. , 1996, Auditory neuroscience.

[81]  Penner Tinnitus Synthesis: Fluctuant and Stable Matches to the Pitch of Tinnitus. , 1995, The international tinnitus journal.

[82]  Jinsheng Zhang,et al.  Plasticity of spontaneous neural activity in the dorsal cochlear nucleus after intense sound exposure , 2000, Hearing Research.

[83]  J. W. House,et al.  Tinnitus: surgical treatment. , 1981, Ciba Foundation symposium.

[84]  S. Otto,et al.  Effects of electrical brainstem stimulation on tinnitus. , 1994, Acta oto-laryngologica.

[85]  T. I. Hempstock,et al.  Study of tinnitus induced temporarily by noise. , 1969, The Journal of the Acoustical Society of America.

[86]  Akira Mitani,et al.  Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat , 1987, Brain Research.

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

[88]  Richard Kempter,et al.  Development of tinnitus‐related neuronal hyperactivity through homeostatic plasticity after hearing loss: a computational model , 2006, The European journal of neuroscience.

[89]  R A Levine,et al.  Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. , 1999, American journal of otolaryngology.