Morphological relationships of peptidergic and noradrenergic nerve terminals to olivocochlear neurones in the rat
Introduction
The olivocochlear bundle in the rat comprises the axons of two groups of auditory efferent neurones that terminate in the cochlea. Lateral olivocochlear neurones project to the nerve fibres beneath the inner hair cells and medial olivocochlear neurones terminate directly on the outer hair cells (Warr and Guinan, 1979). Lateral and medial olivocochlear neurones originate in different subdivisions of the superior olivary complex, i.e. lateral olivocochlear neurones originate ipsilaterally in the lateral superior olive whereas medial olivocochlear neurones originate bilaterally in the ventral nucleus of the trapezoid body (VNTB) (White and Warr, 1983, Vetter et al., 1991, Vetter and Mugnaini, 1992). In general, medial olivocochlear neurones have been shown to have an inhibitory effect on cochlear neural output (Warren and Liberman, 1989, Giraud et al., 1995), but their precise function in hearing is still under investigation. A number of studies have provided evidence for a role of the medial efferents in protection from loud damaging sounds (Rajan, 1988a, Rajan, 1988b, Patuzzi and Thompson, 1991). Recent experimental as well as clinical studies have also suggested a role for medial olivocochlear neurones in the detection of signals in noisy environments (Giraud et al., 1997, Scharf et al., 1997, Hienz et al., 1998).
To gain more insight into the medial olivocochlear system several studies have investigated the microcircuitry within the VNTB. Anatomical studies have demonstrated the presence of a variety of neurotransmitters within the VNTB, such as glycine (Saint-Marie et al., 1989), serotonin (Thompson and Thompson, 1995), γ-aminobutyric acid (Moore and Moore, 1987), substance P, somatostatin (Wynne and Robertson, 1997) and noradrenaline (Wynne and Robertson, 1996). Electrophysiological experiments on in vitro brain slices have demonstrated excitatory effects of substance P, inhibitory effects of leu-enkephalin and both excitatory and inhibitory effects of noradrenaline, serotonin and cholecystokinin on neurones in the VNTB (Wang and Robertson, 1997a, Wang and Robertson, 1997b, Wang and Robertson, 1998a). More specifically, substance P and noradrenaline have been shown to affect medial olivocochlear neurones in the VNTB (Wang and Robertson, 1997b, Wang and Robertson, 1998b). These studies also suggested that the observed effects were established via direct synaptic contacts, rather than being a result of some modulating action of these substances on other neurotransmitters or an interneuronal cell population. However, little morphological evidence is available at present to support these observations. The number of studies investigating the direct relationship of neurotransmitters with medial olivocochlear neurones is very limited. One brief report in the cat suggests that substance P-containing nerve endings contact lateral olivocochlear neurones only (Adams, 1996). In contrast, serotonin-containing processes have been shown anatomically to directly contact medial as well as lateral olivocochlear neurones in the bush baby (Thompson and Thompson, 1995).
In view of the limited studies available, the question remains whether and how noradrenaline as well as the neuropeptides shown to be present in the VNTB provide input to medial olivocochlear neurones in the rat. Do they act directly on the dendrites and/or somata of medial olivocochlear neurones or are interneurones the mediators of any observed effect? The present study examines the morphological relationship between terminals containing noradrenaline, substance P, leu-enkephalin and cholecystokinin and medial olivocochlear neurones in the rat VNTB. To address this question an immunocytochemical double labelling technique was used after intracochlear injections of a retrograde tracer. This method made it possible to simultaneously visualise medial olivocochlear neurones and structures containing markers for noradrenaline and the various neuropeptides.
Section snippets
Animals
Experiments were performed on 27 male Wistar rats weighing 190–230 g. Several of these animals were used to optimise the double labelling techniques used. All experimental protocols conformed to the Code of Practice of the National Health and Medical Research Council of Australia and were approved by the Animal Experimentation Ethics Committee of the University of Western Australia.
Intracochlear injections
Glass pipettes were filled with 1% cholera toxin B subunit (CTB, List Biological Laboratories) in 0.1 M phosphate
Comparison of different retrograde tracers
To optimise the quality of the double labelling protocol we tested two different retrograde tracers, CTB and FG. Intracochlear injections with these tracers and subsequent immunocytochemistry resulted in an identical pattern of neuronal labelling in the superior olivary complex (SOC). Labelled neurones were found in the ipsilateral lateral superior olive (LSO) as well as bilaterally in the VNTB. The neurones in the LSO, the lateral olivocochlear population, have dendrites that are restricted to
Technical considerations
In the present study we used double labelling immunocytochemistry to distinguish retrogradely labelled olivocochlear neurones and their input within the one section. This technique, based on the use of DAB with and without nickel intensification, enabled us to investigate the relationship between medial olivocochlear neurones in the VNTB and fibres and varicosities labelled for substance P, cholecystokinin, leu-enkephalin and dopamine-β-hydroxylase at the light microscopical level. In addition,
Acknowledgements
Supported by grants from the National Health and Medical Research Council, the Medical Research Infrastructure Fund and The University of Western Australia.
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