Elsevier

Hearing Research

Volume 118, Issues 1–2, April 1998, Pages 151-156
Hearing Research

Specific sound-induced noradrenergic and serotonergic activation in central auditory structures

https://doi.org/10.1016/S0378-5955(98)00031-8Get rights and content

Abstract

We have studied the noradrenergic and serotonergic changes induced by white noise stimulation at 70, 90 or 110 dB SPL for 45 min, in cochlear nuclei, inferior colliculus (IC), primary auditory cortex (PAC) and as a comparison in locus coeruleus (LC) and raphe dorsalis using HPLC. Both noradrenergic and serotonergic pathways were activated in the dorsal+posteroventral cochlear nuclei (DCN+PVCN) without changes in the anteroventral cochlear nucleus (AVCN) and IC. In the DCN+PVCN the noradrenergic activation was restricted to animals exposed to 70 dB SPL whereas the increase of serotonin content was intensity-dependent. In PAC serotonergic activation was observed only after 70 dB SPL exposure. These data suggest that in physiological conditions (70 dB SPL) noradrenergic and serotonergic regulation of the processing of auditory information occurs specifically in the dorsal cochlear nucleus where the control of incoming information to higher auditory structures takes place (i.e. IC and PAC). We suggest that the serotonergic activation in the primary auditory cortex for 70 dB SPL sound stimulation could be related to the fact that low-intensity white noise stimulation could be the most plastic-demanding processing in the auditory cortex.

Introduction

The cochlear nuclei, the inferior colliculus (IC) and the primary auditory cortex (PAC) are three station relays for the processing of auditory information in the central nervous system. Each of these structures conveys auditory information using presumably fast excitatory amino-acidergic transmission. The activity of central auditory pathways is modulated by inhibitory inputs (glycine, γ-aminobutyric acid (GABA)) and each of those three structures receives noradrenergic and serotonergic fibres.

Cochlear nuclei contain noradrenergic fibres that have been shown to originate mainly from locus coeruleus in the rat (Kromer and Moore, 1980; Klepper and Herbert, 1991). Biochemical characterisation of this innervation has been detailed elsewhere in the rat at basal state condition, during ageing and compared between pigmented and albino animals (Cransac et al., 1995, Cransac et al., 1996, Cransac et al., 1997b).

Noradrenaline (NA) is present in the IC in noradrenergic fibres originating from locus coeruleus (Kobayashi et al., 1974; Holman et al., 1976). Noradrenergic fibres are slightly more numerous in the dorsal cortex than in other subnuclei of the IC (Klepper and Herbert, 1991).

All areas of the rat neocortex receive noradrenergic innervation from the ipsilateral locus coeruleus. Single noradrenergic fibres branch at all levels and undergo extensive collateralisation (Levitt and Moore, 1978).

Serotonergic innervation of the cochlear nuclei of the rat has been extensively demonstrated (Steinbusch, 1981). In the dorsal cochlear nucleus (DCN), posteroventral and anteroventral cochlear nuclei (PVCN and AVCN), serotonin (5-HT) immunoreactive fibres are evenly distributed across subnuclei. This serotonergic innervation of the cochlear nuclei originates mainly from the dorsal and median raphe region (Klepper and Herbert, 1991; Thompson et al., 1994a).

In the IC of rats serotonergic fibres form a dense network in both the dorsal and external cortices of the IC, whereas they are less abundant in the remaining subnuclei. This serotonergic innervation originates largely in the raphe dorsalis with occasional contribution from serotonergic neurones in other groups of the raphe nuclei (Klepper and Herbert, 1991).

In the PAC many serotonergic baskets surround the somata and dendrites of GABA neurones, suggesting a strong interaction between serotonergic axon terminals and specific GABA neurones (DeFelipe et al., 1991).

We have studied monoamines and metabolite levels in the AVCN, DCN+PVCN, the IC and the PAC after broad-band white noise sound stimulation of different intensities in intact animals in order to evaluate at which site and to what extent noradrenergic and serotonergic fibres are involved in the control of the processing of ascending auditory information.

The effect of sound stimulation was also studied in the locus coeruleus and raphe dorsalis which contain the cell bodies of the noradrenergic and serotonergic projections to central auditory structures (Klepper and Herbert, 1991; Levitt and Moore, 1978; DeFelipe et al., 1991).

NA, 5-HT and their metabolites, 3-methoxy-4-hydroxyphenylglycol (MHPG) and 5-hydroxyindoleacetic acid (5-HIAA), were assayed using high performance liquid chromatography (HPLC). The ratios MHPG/NA and 5-HIAA/5-HT were considered indices of NA and 5-HT turnover respectively (Kohno et al., 1981; Mena et al., 1976).

Section snippets

Materials and methods

Groups of eight Sprague-Dawley male rats (220–270 g) were exposed to white noise at intensities of 70, 90 and 110 dB SPL; the control group was kept in the same room under silent conditions (≤35 dB SPL). White noise stimulation was generated (General Radio 1381 random-noise generator 20 Hz-50 kHz), amplified (amplifier NAD 3240 PE) and delivered through a loudspeaker (acousto-pro driver 3565). The cage where animals were exposed to sound was 0.35 m from the source, thus allowing a good

Results

In the locus coeruleus, the noradrenergic content, MHPG or MHPG/NA did not change regardless of the intensity of the sound stimulation (Table 1).

In the raphe dorsalis there was an accumulation of 5-HIAA for the 70 dB SPL group when compared to 90 and 110 dB SPL groups (Table 1).

In the DCN+PVCN noradrenergic activity was enhanced for 70 dB SPL intensity as evidenced by the increase of the MHPG content and the ratio MHPG/NA (Fig. 1).

Simple linear regression showed that the content of 5-HT in the

Discussion

We have studied central structures (AVCN, DCN+PVCN, IC, PAC) involved in the processing of ascending auditory information which all receive noradrenergic and serotonergic neuromodulatory fibres.

Our data show that sound stimulation was able to induce noradrenergic and serotonergic activation in the DCN+PVCN and serotonergic activation in PAC but no significant changes in AVCN and IC. The striking fact was that most monoaminergic activation, when it did occur, was limited to the group of animals

Acknowledgements

H. Cransac was a grantee of the European Neuroscience Programme 1995 (Grant 201). This study was supported by MFR (Sweden; Contract B95-17X-06578-13A) and INSERM (France). Thanks are due to B.I. Zladsky for animal care, to J. Hörnsten for skilful sound engineering, and to A. Vouillarmet and R.M. Cottet-Emard for biochemical analysis.

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