Olivocochlear neurons in the chinchilla: a retrograde fluorescent labelling study
Introduction
Previous studies of the olivocochlear (OC) system in mammals indicate that the efferent projection to each cochlea arises from neurons located in two distinct zones of the superior olivary complex, lateral and medial. Moreover, across species, the OC neurons in these two zones exhibit clear similarities in cellular morphology, preponderant side of projection and synaptic targets in the organ of Corti (for review, see Warr, 1992). The majority of these efferents are small, lateral OC neurons (LOC) which project predominantly (70–100%) to the ipsilateral cochlea where they synapse with the radial afferent fibers beneath the inner hair cells. The second largest group consists of large, medial OC neurons (MOC), which project predominantly (53–75%) to the contralateral cochlea where they synapse with outer hair cells. Finally, in some rodents, there is a small number of generally larger LOC neurons which closely surround the lateral superior olivary nucleus, for which reason they were named ‘shell’ neurons (Vetter and Mugnaini, 1992). These neurons are of special interest because they form distinctive, bidirectional, longitudinally diffuse, inner spiral and tunnel spiral bundle fibers (Brown, 1987) that terminate beneath the inner hair cells, preponderantly on the side ipsilateral to their origin (Warr et al., 1997).
The chinchilla is a widely used species in studies of the auditory system but the origins and distribution of its OC neurons, as demonstrated by retrograde tracing techniques, has until now not fully been documented. Nevertheless, previous work has explored a number of features of both the LOC and MOC systems in this species, including; (1) the fine structure of efferent synapses beneath the inner and outer hair cells (Smith and Rasmussen, 1963, Gulley and Reese, 1977), (2) the differences in magnitude and distribution between crossed and uncrossed efferents to the outer hair cells (Iurato et al., 1978), (3) the distribution and morphology of acetylcholinesterase (AChE)-stained neurons in the superior olivary complex (Osen et al., 1984), (4) the role of the OC bundle (OCB) in modulating cochlear mechanics (Siegel and Kim, 1982), (5) the role of the OCB in protecting against acoustic trauma (Zheng et al., 1997a, Zheng et al., 1997b), (6) the facilitatory action of opioid peptides contained in OC fibers beneath the inner hair cells (Sahley et al., 1991) and (7) the vulnerability of OC fibers beneath the inner hair cells to cholinergic neurotoxins (Morley et al., 1991).
Prior to the preliminary reports of retrograde labelling of OC efferents in chinchilla (Weekly et al., 1992, Azeredo et al., 1997, Kliment et al., 1997), there was indirect evidence, based on histochemical staining for AChE, on the cells of origin of the OCB in this species (Osen et al., 1984). This study demonstrated small neurons (presumably LOC) within the lateral superior olivary nucleus (LSO) and large neurons (presumably MOC) in the dorsomedial periolivary (DMPO) area. Supplementing these findings were electron microscopic data on the proportion of crossed versus uncrossed efferent innervation in the chinchilla (Iurato et al., 1978). After severing the decussation of the OCB in the brainstem, Iurato and his co-workers found only a slight loss of innervation beneath the inner hair cells, but a large percentage of boutons (81%) on outer hair cells degenerated. Such a large loss of endings was somewhat unexpected since, in the cat, the ratio of the crossed to uncrossed MOCs was closer to 2:1 than the nearly 4:1 observed in the chinchilla (Warr, 1975).
In the present study, we have pooled two independent sets of data, one obtained by investigators in Syracuse (NY, USA)using a double retrograde fluorescent labelling protocol and the other obtained by investigators in Omaha (NE, USA) using a single retrograde fluorescent labelling protocol. The motivation for the two studies differed somewhat in the two locations. In Syracuse, an investigation of the organization of the MOC system in the chinchilla became of interest when efforts to demonstrate the phenomenon of efferent-mediated contralateral sound suppression, either as measured by changes in the compound action potential (CAP) or in distortion product otoacoustic emissions (DPOAE), met with failure (E. Relkin, unpublished observations; D. Henderson, personal communication). Such a contralateral suppression, which is mediated by MOC neurons whose axons do not cross the midline but instead innervate the ear ipsilateral to their side of origin, has been clearly demonstrated in both the cat (Buno, 1978, Murata et al., 1980, Warren and Liberman, 1989, Puria et al., 1996) and the guinea pig (Puel and Rebillard, 1990, da Costa et al., 1997), as well as in man (Mott et al., 1989, Veuillet et al., 1991, Chery-Croze et al., 1993). Since these effects are mediated by the ipsilateral contingent of MOC neurons (Liberman and Brown, 1986, Warren and Liberman, 1989), it was of key importance to confirm the experimental indications that this pathway supplied only some 20% of efferent terminals beneath the outer hair cells (Iurato et al., 1978).
In Omaha, the motivation was to determine how the chinchilla’s efferent system is organized and how it compares to that of other mammals, generally, and more specifically, whether dual populations of LOC neurons, intrinsic and shell, were present in this species, as observed in the rat (Vetter and Mugnaini, 1992, Warr et al., 1997).
Section snippets
Materials and methods
Adult male chinchillas weighing 400–550 g were used. In Syracuse (a collaboration at the Syracuse University and the Health Science Center of the State University of New York at Syracuse), five chinchillas were anesthetized with a mixture of acepromazine and ketamine (1.0 cc/kg), injected intramuscularly. The tympanic membrane was removed to expose the middle and apical turns of the cochlea. The round window was punctured and gelfoam soaked in a neuronal tracer solution was packed into the
General observations
Tracer injections into the scala tympani produced a consistent pattern of retrograde labelling in the superior olivary complex (Fig. 1) and a somewhat less consistent pattern of labelling in other locations, as will be described at the end of Section 3. The pattern in the superior olivary complex consisted of numerous, mostly small neurons, in the ipsilateral LSO and a lesser number of larger neurons in the DMPO region, mainly on the side contralateral to the injection. In addition, a small
MOC system
MOCs were found in DMPO and RPO bilateral to the cochlear tracer infusion. The difference between the number of cells labelled between the Omaha and Syracuse groups (Table 2a, Table 2b, Table 2c), while possibly a function of survival time, cannot be completely accounted for. The majority of the MOCs were found in DMPO. The chinchilla is unusual in this respect, as the mustache bat is the only other known species with virtually all of its MOCs in this peri-olivary nucleus and few in the ventral
Acknowledgements
Supported by NIH Grants 5 P60 DC00982 (MJK, BJM, WBW and JMW) and 2 PO1 DC00215 (WBW) and to BTNRH and by NIH Grant 2PO1 DC00380-09A2 (NBS and ER). We thank JoEllen Boche for her expert histological work and Skip Kennedy and Diane Schmidt of the BTNRH Media/Graphics Department for their work on the drawings and digital images in Fig. 1, Fig. 2, Fig. 5.
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