Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss

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Abstract

Increase in spontaneous neural activity after noise-induced hearing loss has frequently been associated with the phenomenon of tinnitus. Eighteen juvenile and adult cats were exposed for 2 h to a 6 kHz tone with an intensity of 115 dB SPL at the cat’s head. Seven non-exposed littermates and seven other normal hearing cats were used as age-matched controls. The trauma cats showed localized hearing losses, as assessed by ABR, ranging from less than 20 to 60 dB. The frequency representation in primary auditory cortex was mapped using an eight-electrode array. Single-unit spontaneous activity was recorded for 15 min. Peak cross-correlation coefficients (R) for unit cluster activity recorded on separate electrodes were calculated. We found elevated spontaneous firing rates in regions with reorganization of the tonotopic map compared to the neurons in the non-reorganized cortical regions in the same animals. A second finding was that in these regions the peak cross-correlation coefficients were also increased relative to the non-reorganized parts. A third finding was that exposed animals showed higher spontaneous activity compared to controls regardless of the presence of cortical reorganization. This may be a correlate of tinnitus in the presence of only minor hearing losses.

Introduction

Changes of spontaneous neural activity after noise-induced hearing loss have been reported in various parts of the auditory system and have frequently been associated with the phenomenon of tinnitus (Kiang et al., 1970, Brozoski et al., 2002). In case only outer hair cell stereocilia were damaged, an increase in spontaneous firing rate and a hypersensitive tail of the frequency tuning curve was found after acute noise trauma (Liberman and Dodds, 1987). In auditory nerve fibers that no longer responded to sound after noise trauma, Liberman and Kiang (1978) found depressed spontaneous activity. This reduction in spontaneous activity was correlated with a selective loss of the tallest row of stereocilia from the inner hair cells (Liberman and Dodds, 1984). A comparable reduction in the spontaneous firing rates of ventral cochlear nucleus (VCN) neurons after noise trauma was reported by Salvi et al. (1978). In sharp contrast, the spontaneous activity in the dorsal cochlear nucleus (DCN) was elevated nearly 10-fold after noise trauma (Kaltenbach and McCaslin, 1996). This spontaneous activity increase appeared to be a slowly developing phenomenon that emerged between 2 and 5 days after exposure (Kaltenbach et al., 2000) and appeared to be largely due to changes in fusiform cell activity (Brozoski et al., 2002). Sharply decreased glutamic acid decarboxylase activity, suggesting a reduction in the gamma-aminobutyric acid (GABA) levels, was found in the inferior colliculus after intense noise exposure (Milbrandt et al., 2000). This could result in increased spontaneous activity. Increases in spontaneous firing rates relative to normal parts of primary auditory cortex (AI) were found in regions with reorganization of the tonotopic map induced by exposure to loud pure tones (Eggermont and Komiya, 2000). These findings suggest that, except for cells in VCN, permanent hearing loss resulting from noise trauma is accompanied by an increase in spontaneous activity in auditory nuclei and cortex. This increase appears to be much larger in the DCN (about a 10-fold increase) than in AI (about a factor two increase). Reorganization of cortical tonotopic maps and increased spontaneous activity is frequently associated with tinnitus (Rauschecker, 1999, Syka, 2002).

After a less than 20 dB localized hearing loss resulting from noise trauma (Rajan, 1998, Rajan, 2000) a strong reduction in the surround inhibition was reported. This was inferred from increased frequency tuning curve bandwidths. This reduced inhibition may also play a role in the increased spontaneous activity. Recently we reported (Seki and Eggermont, 2002) the effects of minor to moderate hearing loss on potential changes in cortical tonotopic maps. We found a variety of hearing loss configurations, whereby an average hearing loss above 20 dB in the frequency range above 6 kHz consistently produced cortical tonotopic map changes, but sometimes only in a limited frequency range. Considerable broadening of frequency tuning curves was observed, and was associated with increased characteristic frequency (CF) thresholds, in regions of localized hearing loss and attributed to the unmasking of excitation from neighboring frequency regions.

In the present study we report on the changes in spontaneous activity and in neural synchrony in the AI of these same cats reported in Seki and Eggermont (2002), and relate these changes to the presence or absence of reorganization of the tonotopic map.

Section snippets

Animal preparation

The care and the use of animals reported on in this study were approved (#P88095) by the Life and Environmental Science Animal Care Committee of the University of Calgary. Cats were premedicated with 0.25 ml/kg body weight of a mixture of 0.1 ml acepromazine (0.25 mg/ml) and 0.9 ml of atropine methyl nitrate (5 mg/ml) administered subcutaneously. After about 30 min they received an intramuscular injection of 25 mg/kg of ketamine (100 mg/ml) and 20 mg/kg of sodium pentobarbital (65 mg/ml).

Results

The data for this paper were obtained from the same cats for which the tonotopic map changes and the changes in frequency tuning curves were reported in Seki and Eggermont (2002). Eighteen cats were exposed to the trauma tone and 14 control cats (including seven non-exposed littermates) were used as age-matched controls. At the time of recording the control cats were on average 130±17 days old and the exposed cats were 137±34 days old. The amount of peripheral hearing loss induced by the pure

Discussion

The main effect of a localized hearing loss induced by exposure to a loud pure tone is elevated spontaneous firing rates in regions with reorganization of the tonotopic map compared to the non-reorganized parts in the same animals. This confirms earlier findings of Eggermont and Komiya (2000). A second finding was that in these regions the peak cross-correlation coefficient was also increased relative to the non-reorganized parts. In a previous paper Eggermont and Komiya (2000), using dual

Acknowledgements

This work was supported by the Alberta Heritage Foundation for Medical Research, the National Sciences and Engineering Research Council, the American Tinnitus Association, and the Campbell McLaurin Chair for Hearing Deficiencies. Pamela Valentine and Arnaud Noreña assisted in the data collection. Greg Shaw provided programming assistance.

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