An auditory negative after-image as a human model of tinnitus

Human Brain Mapping

Several studies have demonstrated the neural correlates of chronic tinnitus. However, we still do not understand what happens in the acute phase. Past studies have established Zwicker tone (ZT) illusions as a good human model for acute tinnitus. ZT illusions are perceived following the presentation of a notched noise stimulus, that is, broadband noise with a narrow band-stop filter (notch). In the current study, we compared the neural correlates of the reliable perception of a ZT illusion to that which is not. We observed changes in evoked and total theta power in widespread regions of the brain particularly in the temporal-parietal junction, pregenual anterior cingulate cortex/ventromedial prefrontal cortex (pgACC/vmPFC), parahippocampus during perception of the ZT illusion. Furthermore, we observe that increased theta power significantly predicts a gradual positive change in the intensity of the ZT illusion. Such changes may suggest a malfunction of the sensory gating system that enables habituation to redundant stimuli and suppresses hyperactivity. It could also suggest a successful retrieval of the memory of the missing frequencies, resulting in their conscious perception indicating the role of higher-order processing in the mechanism of action of ZT illusions. To establish a more concrete relationship between ZT illusion and chronic tinnitus, future longitudinal studies following up a much larger sample of participants who reliably perceive a ZT illusion to see if they develop tinnitus at a later stage is essential. This could inform us if the ZT illusion may be a precursor to chronic tinnitus.

JARO-Journal of the …, 2008

Animals exposed to noise trauma show augmented synchronous neural activity in tonotopically reorganized primary auditory cortex consequent on hearing loss. Diminished intracortical inhibition in the reorganized region appears to enable synchronous network activity that develops when deafferented neurons begin to respond to input via their lateral connections. In humans with tinnitus accompanied by hearing loss, this process may generate a phantom sound that is perceived in accordance with the location of the affected neurons in the cortical place map. The neural synchrony hypothesis predicts that tinnitus spectra, and heretofore unmeasured "residual inhibition functions" that relate residual tinnitus suppression to the center frequency of masking sounds, should cover the region of hearing loss in the audiogram. We confirmed these predictions in two independent cohorts totaling 90 tinnitus subjects, using computer-based tools designed to assess the psychoacoustic properties of tinnitus. Tinnitus spectra and residual inhibition functions for depth and duration increased with the amount of threshold shift over the region of hearing impairment. Residual inhibition depth was shallower when the masking sounds that were used to induce residual inhibition showed decreased correspondence with the frequency spectrum and bandwidth of the tinnitus. These findings suggest that tinnitus and its suppression in residual inhibition depend on processes that span the region of hearing impairment and not on mechanisms that enhance cortical representations for sound frequencies at the audiometric edge. Hearing thresholds measured in age-matched control subjects without tinnitus implicated hearing loss as a factor in tinnitus, although elevated thresholds alone were not sufficient to cause tinnitus.

Neuroreport, 2002

Acta Oto-Laryngologica, 2006

Conclusions: Psychoacoustic functions relating the depth and duration of tinnitus suppression ('residual inhibition') to the center frequency of band-passed noise masking sounds appear to span the region of hearing loss, as do psychoacoustic measurements of the tinnitus spectrum. The results (1) suggest that cortical map reorganization induced by hearing loss is not the principal source of the tinnitus sensation and (2) provide a necessary baseline for optimizing residual inhibition in individual cases. Objective: To measure residual inhibition functions and tinnitus spectra using sounds spanning the region of hearing loss. Materials and methods: Three subject-driven, computer-based tools were developed and applied to measure psychoacoustic properties of tinnitus and residual inhibition in 32 subjects with chronic tonal, ringing, or hissing tinnitus. Residual inhibition functions were measured with band-passed noise sounds varying in center frequency up to 12.0 kHz. Results: The depth and duration of residual inhibition increased with the center frequency of the band-passed noise stimuli. Near-elimination of tinnitus for up to 45 s was reported by 8/24 (33%) subjects at center frequencies above 3 kHz (these cases distributed across tinnitus types). Tinnitus spectra covered the region of hearing loss with no preponderance of frequencies near the audiometric edge of normal hearing.

IFAC Proceedings Volumes, 2003

Lateral-inhibitory-networks (LINs) of neurons enhance edges and peaks in their input excitation pattern. In the case of reduced spontaneous input to a region of a LIN, the edges between the normal and abnormal spontaneous input will be enhanced in the LIN's output. In LINs within the central auditory system, regional reduction of spontaneous input may occur because of deafferentation resulting from a peripheral hearing loss. A model of auditory LINs is developed to investigate how such abnormal spontaneous edges in LIN outputs could be related to tinnitus, the phantom perception of sounds.

Physical Review Letters, 2003

The Zwicker tone is an auditory aftereffect. For instance, after switching off a broadband noise with a spectral gap, one perceives it as a lingering pure tone with the pitch in the gap. It is a unique illusion in that it cannot be explained by known properties of the auditory periphery alone. Here we introduce a neuronal model explaining the Zwicker tone. We show that a neuronal noise-reduction mechanism in conjunction with dominantly unilateral inhibition explains the effect. A pure tone's ''hole burning'' in noisy surroundings is given as an illustration.

Although a peripheral auditory (bottom-up) deficit is an essential prerequisite for the generation of tinnitus, central cognitive (top-down) impairment has also been shown to be an inherent neuropatho-logical mechanism. Using an auditory oddball paradigm (for top-down analyses) and a passive listening paradigm (for bottom-up analyses) while recording electroencephalograms (EEGs), we investigated whether top-down or bottom-up components were more critical in the neuropathology of tinnitus, independent of peripheral hearing loss. We observed significantly reduced P300 amplitudes (reflecting fundamental cognitive processes such as attention) and evoked theta power (reflecting top-down regulation in memory systems) for target stimuli at the tinnitus frequency of patients with tinnitus but without hearing loss. The contingent negative variation (reflecting top-down expectation of a subsequent event prior to stimulation) and N100 (reflecting auditory bottom-up selective attention) were different between the healthy and patient groups. Interestingly, when tinnitus patients were divided into two subgroups based on their P300 amplitudes, their P170 and N200 components, and annoyance and distress indices to their tinnitus sound were different. EEG theta-band power and its Granger causal neurodynamic results consistently support a double dissociation of these two groups in both top-down and bottom-up tasks. Directed cortical connectivity corroborates that the tinnitus network involves the anterior cingulate and the parahippocampal areas, where higher-order top-down control is generated. Together, our observations provide neurophysiological and neurodynamic evidence revealing a differential engagement of top-down impairment along with deficits in bottom-up processing in patients with tinnitus but without hearing loss.

Journal of Advanced Medical Sciences And Applied Technologies, 2016

Our knowledge about subjective tinnitus physiopathology has improved in the last decades, while information to understand the main mechanisms that transform a neutral phantom sound to tinnitus distress appear to be inadequate. The current review presents evidence from several studies using neuroimaging, electrophysiology and brain lesion techniques aiming at hypothesizing a new realistic multimodality tinnitus framework which can better explain the structural and functional brain connectivity in different stages of tinnitus development. Further to the present work, a full review of the entire literature should be prompted to discuss evidence to more comprehensively investigate the relationship between structural and functional connectivity of tinnitus. Progresses in such framework will shed lights to the tinnitus neurofunctional model and further evidence-based treatment modalities.

Frontiers in Systems Neuroscience, 2012

Frontiers in Neuroscience, 2016