The neuroscience of tinnitus

2004, Trends in Neurosciences

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7 pages

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AI-generated Abstract

Tinnitus is a distressing auditory phantom sensation often linked to hearing loss due to aging or noise exposure. Recent neuroscience research has begun to dissect the neural mechanisms that underlie this phenomenon, primarily focusing on intracortical inhibition and the brain's role in generating the sensation when external sound is absent. Despite various management strategies, no reliable treatment exists for completely eliminating tinnitus, underscoring the need for further understanding and innovative approaches in its prevention and management.

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Figure 1. Schematic outline of the auditory system. This figure excludes binaural pathways and interhemispheric connections, but indicates parts where tinnitus- related studies have been conducted (yellow). Sound activates the outer hair cells (OHC) and inner hair cells (IHC) in the cochlea (bottom). The cochlea decomposes multi-frequency signals into a spatial output organized according to frequency; this is tonotopic mapping. The OHC act mainly as amplifiers of the mechanical movement of the basilar membrane, thereby sharpening the frequency resolution and enhancing sensitivity. Their working point and effectiveness are under control of the central auditory system (CAS), through olivocochlear bundle feedback (dark blue lines) from the superior olivary complex (SOC). The IHC are the mechanoelectric transducers (microphones) in the cochlea, whose neural output forms the auditory nerve. Auditory nerve fibers bifurcate to send collaterals into both the ventral cochlear nucleus (VCN) and dorsal cochlear nucleus (DCN); both structures show tonotopic maps. Such mappings are found throughout the CAS and the nerve fiber tracts that propagate this frequency-specific information by the lemniscal pathway (thick black lines). The DCN, in addition to auditory nerve input, is also innervated by fibers from various parts of the somatosensory system (cyan), so this structure is a multi-modal processing station that is probably heavily involved in tinnitus resulting from, for example, orofacial movements and gaze changes. For that reason, this structure is considered here to be part of the extralemniscal pathway (green). Other parts of the extralemniscal pathway are the lateral nucleus (LN) and external nucleus (ICx) of the inferior colliculus, parts of the medial geniculate body (MGB) in the thalamus, and the secondary auditory cortex (All), which are all characterized by sensitivity to somatosensory stimuli. The MGB and auditory cortical areas project to the amygdala (top left), which is associated with fear conditioning and emotional processing. The CAS is characterized by strong reciprocal connections between various structures, and the descending parts consist of interconnected feedback loops that allow the cortex to modulate activity of the entire subcortical CAS. There are strong direct feedback connections between primary auditory cortex (Al) and DCN, as well as from auditory cortical areas via the central nucleus of the inferior colliculus (ICc). Thus, changes in cortical activity as a result of a loss of inhibition could change the subcortical activity in the ICc and DCN (directly) and even in the cochlea (indirectly via the olivocochlear bundle). Changes in the DCN, in turn, will directly affect the processing of lemniscal activity at the level of the VCN and the ICc. Thus, there could be a synergy between changes occurring in the cortex and those in the brainstem.

*Rate and synchrony (synch.) of spontaneous activity in parts of the auditory system can be affected by drugs and noise trauma. ¢ indicates a significant increase, | indicates significant decrease and = indicates no change. ‘Yes’ indicates that tinnitus has been signaled behaviorally after administration of the drug or trauma. Abbreviation: NS, not studied. Table 1. Effects of drugs and trauma on spontaneous auditory activity and tinnitus*”

Figure 2. Normal and reorganized tonotopic maps in primary auditory cortex (Al). (a) The characteristic frequency at each recording site is color-coded and overlaid on a photograph of the cortical surface for a control cat (i) and a cat with a noise induced hearing loss (ii). The hearing loss was limited to frequencies > 10 kHz and amounted to 3 dB at 12 kHz, 12 dB at 16 kHz, 22 dB at 24 kHz and 23 dB at 32 kHz. (244 and 245 are cat identification numbers.) (b) The effect of restricted high-frequency hearing loss on the input to pyramidal cells (numbered 1-13) in auditory cortex. The large colored arrow shows the normal frequency gradient of the inputs conveying the tonotopic mapping. The thin vertical lines leading to the cortical cells are color-coded to reflect their frequency-specific input from the thalamus. For the higher frequencies, covering the range of the hearing loss, the lines are shown as dashed to indicate their reduced ability to activate cortical cells at low stimulus levels and during silence. Numerous divergent connections lead from each thalamic cell to a range of cortical cells (indicated by lines with the same color). A few inhibitory feedforward connections are indicated [one is labeled (i) on the left]. These affect the same cells that receive their thalamic inputs. Feedback inhibition is also prevalent but is only shown for cell 1 (ii). The assumption is that loss of input limits not only the excitation but also, even more strongly, the inhibitory feedforward activity. As a result, the diverging thalamic inputs from neighboring unaffected cells, and the inputs from cortical cells via horizontal fibers, face less competition from inhibition at those cortical cells deprived from thalamic input. Thus, these excitatory inputs are disinhibited or ‘unmasked’ and can impose their own frequency-selective inputs on cortical cells in the hearing loss range, which will ultimately result in a reorganization of the tonotopic map in the hearing-loss animal. Abbreviations: AES, anterior ectosylvian sulcus; PES, posterior ectosylvian sulcus.

Figure 3. Estimated tinnitus spectrum in relation to hearing loss in four tinnitus subjects. The subjects are representative of ten subjects tested, all reporting tonal tinnitus Etiology was auditory trauma (subjects 6 and 7), sudden hearing loss (subject 4, tinnitus for one year) or unknown (subject 8, tinnitus of three years). Hearing thresholds were measured in 500 Hz steps from 0.5 kHz to 8.0 kHz [up to 14 kHz when hearing loss at 8 kHz did not exceed 70 dB sound pressure level (SPL)] using a staircase method. Afte threshold determination, subjects adjusted the intensity of tones within the studied frequency range (one randomly selected tone at a time) to match the loudness of thei tinnitus. Subjects then stated whether the frequency corresponded to one of the components of their tinnitus spectrum and, if it did, gave a rating on a 10-point scale (10=tinnitus) of the extent to which the frequency was part of their tinnitus sensation. Frequencies were selected randomly from the tested range and repeated until a total o three measurements had been obtained for each frequency. Tones were presented monaurally either to the tinnitus ear (subjects 4, 6 and 7, unilateral cases) or to the ea where tinnitus was most pronounced (subject 8, a bilateral case). In each of the ten cases tested, the rated tinnitus spectrum spanned the region of hearing loss with nc preponderance of edge-frequency ratings. Adapted from Ref. [54].