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The role of central nervous system plasticity in tinnitus - PubMed

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The role of central nervous system plasticity in tinnitus

James C Saunders. J Commun Disord. 2007 Jul-Aug.

Abstract

Tinnitus is a vexing disorder of hearing characterized by sound sensations originating in the head without any external stimulation. The specific etiology of these sensations is uncertain but frequently associated with hearing loss. The "neurophysiogical" model of tinnitus has enhanced appreciation of central nervous system (CNS) contributions. The model assumes that plastic changes in the primary and non-primary auditory pathways contribute to tinnitus with the former perhaps sustaining them, and the latter contributing to perceived severity and emotionality. These plastic changes are triggered by peripheral injury, which results in new patterns of brain activity due to anatomic alterations in the connectivity of CNS neurons. These alterations may change the balance between excitatory and inhibitory brain processes, perhaps producing cascades of new neural activity flowing between brainstem and cortex in a self-sustaining manner that produces persistent perceptions of tinnitus. The bases of this model are explored with an attempt to distinguish phenomenological from mechanistic explanations.

Learning outcomes: (1) Readers will learn that the variables associated with the behavioral experience of tinnitus are as complex as the biological variables. (2) Readers will understand what the concept of neuroplastic brain change means, and how it is associated with tinnitus. (3) Readers will learn that there may be no one brain location associated with tinnitus, and it may result from interactions between multiple brain areas. (4) Readers will learn how disinhibition, spontaneous activity, neural synchronization, and tonotopic reorganization may contribute to tinnitus.

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Figures

Fig. 1
Fig. 1

A. A transmission electron micrograph through the shaft of a normal stereocilium showing the vertical actin filaments with a hint of the horizontal cross bridges. B. and C. Micrographs of overstimulated stereocilia with B showing mild disassembly of the actin/cross bridge matrix and C showing more severe damage (modified from Saunders et al., 1991). D. A micrograph of the stereocilia ankle region where it articulates with the top of the hair cell. The left and right hairs show actin filament deterioration in this area, while the hair to the right has broken from its rootlet (arrow) (from Tilney et al., 1982).

Fig. 2
Fig. 2

Click stimulus input/output evoked response functions in young mice recorded from the CN and IC. Data obtained from a group of overstimulated and control animals nine days post exposure. Hyperactivity in the exposed animals is apparent at high stimulus levels (redrawn from Saunders et al., 1972).

Fig. 3
Fig. 3

Spontaneous activity along the surface of the hamster DCN in groups of overstimulated animals between 2 and 180 days post exposure. After 2 days the activity increased considerably, exhibited some selectivity with regard to DCN location, and was sustained for at least 180 days (redrawn from Kaltenbach et al., 2000).

Fig. 4
Fig. 4

Neural wiring diagram of the dorsal cochlear nucleus showing inhibitory and excitatory inputs, and the interaction of interneurons. See text for explanation of inhibitory influences (permission from Kaltenbach et al., 2005).

Fig. 5
Fig. 5

Top two panels show the surface of the cat auditory cortex (AI). Superimposed on the cortex are the characteristic frequencies detected at different locations. The left panel shows a control animal and the right from a sound damaged animal with cochlear damage above 10.0 kHz. The tonotopic map of the damaged animals is modified with tonotopic representation absent for frequencies above 10.0 kHz (top panels permission from Eggermont, 2005). The bottom left panel (IC) shows tonotopic organization in the IC of a chinchilla with a hearing loss above 1.0 kHz. The black bar shows the frequency extent of the lesion and hearing loss. The solid line and the 95% confidence intervals depict the tonotopic progression with IC depth in normal animals. The black dots indicate tonotopic progression with depth in the exposed animals. The frequency increases as depth increases to about 2.4 mm. Deeper penetrations reveal that the CF of units remains fixed at around 1.0 kHz. This represents tonotopic reorganization of the IC (redrawn from Salvi et al., 2000). The right lower panel shows the change in CF with progressive distance along the auditory cortex in control animals and in cats with inner ear damage above 19.0 kHz (the black bar again shows the extent of the lesion). The control cats show a normal increase in CF as more distal locations are sampled. In the exposed animals the area above 18.0 kHz is only responsive to frequencies at the edge of the lesion (redrawn from Rajan and Irvine, 1998b; Rauschecker, 1999).

Fig. 6
Fig. 6

A Cartoon of how cochlear damage unmasks lateral axonal connections from MGB cells lying at the low frequency edge of the lesion. Neuroplastic changes in spontaneous activity and neuron synchronization in the auditory cortex may arise because of deafferentation and disinhibition of the fiber tracks coming out of the peripheral ear. See text for details (redrawn and modified from Eggermont, 2005).

Fig. 7
Fig. 7

PET images from a patient with a CVA that abolished tinnitus. A. A coronal section. B. and C. Horizontal sections at different depths. The lesion affected white matter in the cortical radiations between the thalamus and auditory cortex, and in more extensive non-sensory tracks (modified from Lowery et al., 2004).

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References

    1. Abbott SD, Hughes LF, Bauer CA, Salvi R, Caspary DM. Detection of glutamate decarboxylase isoforms in rat inferior colliculus following acoustic exposure. Neuroscience. 1999;93:1375–1381. - PubMed
    1. Baguley DM. Mechanisms of tinnitus. British Medical Bulletin. 2002;63:195–212. - PubMed
    1. Bashtanov ME, Goodyear RJ, Richardson GP, Russel IJ. The mechanical properties of the chick (Gallus domesticus) sensory hair bundles: Relative contributions of structures sensitive to calcium chelation and subtilisin treatment. Journal of Physiology. 2004;559:287–299. - PMC - PubMed
    1. Bauer CA. Effects of chronic salicylate on GABAergic activity in the rat inferior colliculus. Hearing Research. 2000;147:175–182. - PubMed
    1. Bauer CA. Mechanisms of tinnitus generation. Current Opinions in Otolaryngology: Head and Neck Surgery. 2004;12:413–417. - PubMed

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