Ringing ears: the neuroscience of tinnitus

Abstract

Tinnitus is a phantom sound (ringing of the ears) that affects quality of life for millions around the world and is associated in most cases with hearing impairment. This symposium will consider evidence that deafferentation of tonotopically organized central auditory structures leads to increased neuron spontaneous firing rates and neural synchrony in the hearing loss region. This region covers the frequency spectrum of tinnitus sounds, which are optimally suppressed following exposure to band-limited noise covering the same frequencies. Cross-modal compensations in subcortical structures may contribute to tinnitus and its modulation by jaw-clenching and eye movements. Yet many older individuals with impaired hearing do not have tinnitus, possibly because age-related changes in inhibitory circuits are better preserved. A brain network involving limbic and other nonauditory regions is active in tinnitus and may be driven when spectrotemporal information conveyed by the damaged ear does not match that predicted by central auditory processing.

Figures

Figure 1.

a–c, Cortical map reorganization (a, b) and psychoacoustic properties (c) of tinnitus. a, In the normal-hearing cat (◊), the characteristic frequency tuning of neurons at low sound intensity shows an orderly gradient from low to high frequencies across the surface of A1 (tonotopy). In cats exposed to noise trauma (+), neurons in the hearing loss region (above ∼8 kHz in this example) responded preferentially to sound frequencies at the edge of normal hearing (from Eggermont and Komiya, 2000, with permission). b, Model for map reorganization in primary auditory cortex. The dashed lines represent diminished thalamocortical input to cortical cells in the hearing loss region. A few inhibitory feedforward connections are indicated (one is labeled i) that suppress the same cells receiving thalamic inputs after one synaptic delay. Feedback inhibition is indicated by one example (ii). Hearing loss reduces excitation and feedforward inhibition arising from thalamocortical pathways, such that the affected neurons begin to respond preferentially to inputs from their unaffected neighbors via horizontal connections in the tonotopic map. The output of the affected neurons remains intact and is heard in terms of their original cochleotopic tuning as the tinnitus percept (from Eggermont and Roberts, 2004, with permission). c, The group-averaged audiogram, tinnitus spectrum, and RI function in 47 participants with chronic bilateral tinnitus. To obtain the tinnitus spectrum, participants rated each of 11 sounds differing in center frequency for similarity to their tinnitus (a likeness rating >40 indicated a sound beginning to resemble tinnitus). The RI function shows the suppression of tinnitus reported after cessation of band-limited noise sounds differing in center frequency (−5 equaled “tinnitus gone;” 0, no change; +5, tinnitus worse). The RI function is plotted negative up to show its similarity to the tinnitus spectrum. WN, white noise (from Roberts et al., 2008, with permission).