Elsevier

Hearing Research

Volume 185, Issues 1–2, November 2003, Pages 65-76
Hearing Research

Anatomy of olivocochlear neurons in the hamster studied with FluoroGold

https://doi.org/10.1016/S0378-5955(03)00213-2Get rights and content

Abstract

The golden hamster (Mesocricetus auratus) is often used in auditory research, but little is known about the anatomical organization of its olivocochlear (OC) neurons, the source of the efferent innervation of the organ of Corti. Accordingly, we labeled the OC neurons projecting to one cochlea by means of retrograde axonal transport of FluoroGold®. In four animals, all labeled OC neurons were counted and digital images of the labeling were captured and analyzed morphometrically. In one case, a 3D computer reconstruction of the bilateral distribution of OC neurons was made. The largest group of OC neurons was comprised by small, intrinsic lateral OC neurons within the ipsilateral lateral superior olivary nucleus (LSO), almost all of which (97%) were located ipsilaterally. The second largest group consisted of medial OC neurons in the ventral nucleus of the trapezoid body, 75% of which were located contralaterally. The smallest group consisted of shell neurons surrounding the LSO, 80% of which projected ipsilaterally. These three types of neurons are generally similar in morphology and distribution to those previously described in the rat and the chinchilla. However, there were several unique findings, including the fact that the hamster possesses the smallest total number of OC neurons (mean 341) of any rodent yet studied.

Introduction

In nearly all mammals, the olivocochlear (OC) neurons form two distinct efferent systems, lateral and medial, that originate in the lateral and medial regions of the superior olivary complex and that innervate, respectively, the inner versus outer hair cells of the cochlea (for review, see Warr, 1992). The functional role of these systems is, in general terms, to reflexively modulate the sensitivity of receptor mechanisms operating in relation to each type of hair cell within the organ of Corti (for reviews, see Guinan, 1996, Veuillet et al., 1999, Le Prell et al., 2001, Fuchs, 2002, Puel et al., 2002).

Lateral olivocochlear (LOC) neurons are situated close to or within the lateral superior olivary nucleus (LSO) and project by means of unmyelinated axons mainly to the ipsilateral cochlea where they synapse primarily with radial afferent fibers beneath the inner hair cells. Medial olivocochlear (MOC) neurons are situated in the medial region of the superior olivary complex and project by means of myelinated axons mainly to the contralateral cochlea, where they synapse directly with outer hair cells. In addition to their projections to the cochlea, MOC neurons (Brown et al., 1991) send axon collaterals into the ventral cochlear nucleus, which appear to compensate for the suppressive effects that MOC neurons exert in the periphery (Benson and Brown, 1990, Kim et al., 1995, Mulders et al., 2003).

The inputs to LOC neurons originate almost exclusively from the ipsilateral cochlear nucleus. Those to MOC neurons are somewhat more complex, and include predominantly contralateral projections from the cochlear nuclei as well as descending fibers from the inferior colliculus and the auditory cortex (Mulders and Robertson, 2000, Xiao and Suga, 2002). The inputs descending from higher levels are thought to underlie the possible involvement of the MOC system in selective attention (Dewson, 1968, Oatman and Anderson, 1977, Scharf et al., 1997). Vetter and co-workers discovered a new type of OC neuron in the rat, shell neurons, which surround the LSO (Vetter et al., 1991, Vetter and Mugnaini, 1992). The existence of a similar cell type has been confirmed in the chinchilla (Azeredo et al., 1999) and the cat (Warr et al., 2002). These neurons, considered a subgroup of LOC neurons since they innervate the inner hair cell region (Warr et al., 1997), have recently also been shown to send collaterals into the ventral cochlear nucleus of the rat (Horvath et al., 2000).

The efferent innervation in the golden hamster has been the subject of a series of studies aimed at determining the temporal sequence of neurodevelopment of the LOC and MOC systems (Simmons et al., 1990, Simmons et al., 1996a, Simmons et al., 1996b, Simmons et al., 1999, Simmons and Raji-Kubba, 1993, Simmons, 1994, Raji-Kubba et al., 2002). These studies have provided presumptive evidence concerning the location and types of OC neurons in the hamster, but these cells have yet to be positively labeled, counted, measured, and their respective patterns of ipsilateral versus contralateral projections determined. A need for such information became apparent in our own laboratory in connection with studies of a strain of hamsters which are subject to audiogenic seizures and exhibit morphological changes both in the cochlea and in the cell body of MOC neurons (Cantos et al., 1996, López et al., 1999). Accordingly, we undertook a comprehensive morphological analysis of the OC neurons in the hamster based on labeling with the sensitive retrograde tracer FluoroGold® (FG). Our report also includes a three-dimensional (3D) reconstruction of the topographic distribution of the OC neurons in the brainstem.

Section snippets

Animals and surgical procedures

Five adult golden hamsters (Mesocricetus auratus) (Charles River Labs, Barcelona, Spain) were used in this study. Animals were handled and experiments were conducted according to the guidelines of the European Communities Council Directive (86/609/EEC) and the current Spanish legislation for the use and care of laboratory animals (BOE 67/8509-12, 1998).

The hamsters were anesthetized with an intramuscular injection of a mixture of ketamine chlorohydrate (Imalgene®) and xylazine (Rompun®). The

Results

The injection of FG into the left cochlea of the hamsters resulted in the labeling of all three types of OC neurons bilaterally in the superior olivary complex. Sections of the injected cochlea confirmed that, in the two cochleae examined, FG had reached the entire basal–apical extent of the organ of Corti. As anticipated from the results in other rodents, we found the two fundamental types of OC neurons: (a) intrinsic LOC neurons, situated within the neuropil of the LSO, mainly (almost

Discussion

We have described the morphology and number of OC neurons in the hamster and created a 3D reconstruction of their distribution in the superior olivary complex. Overall, our findings confirm, by means of specific retrograde labeling from the cochlea, that the hamster does possess the same three basic types of OC neurons found in several other rodent and non-rodent species, and that they have rather similar locations and proportional distributions as found in other rodents. However, it was

Acknowledgements

The authors wish to thank Mr. Ignacio Plaza for excellent technical assistance in the histological procedures, and Mr. Juan Carlos Andaluz, who kindly helped with the 3D reconstruction software. M.A.S.G. was supported by a scholarship from the Instituto de Neurociencias de Castilla y León. W.B.W. was supported by NIH Grant NIDCD DC00215. D.E.L. was supported by Grants FIS PI021697 and JCyL-UE SA084/01.

References (47)

  • D.D. Simmons et al.

    Postnatal calcitonin gene-related peptide in the superior olivary complex

    J. Chem. Neuroanat.

    (1993)
  • D.D. Simmons et al.

    Olivocochlear innervation of inner and outer hair cells during postnatal maturation: an immunocytochemical study

    Dev. Brain Res.

    (1996)
  • W.B. Warr et al.

    Efferent innervation of the inner hair cell region: origins and terminations of two lateral olivocochlear systems

    Hear. Res.

    (1997)
  • E.H. Warren et al.

    Effects of contralateral sound of auditory-nerve responses. I. Contributions of cochlear efferents

    Hear. Res.

    (1989)
  • A. Aschoff et al.

    Different origins of cochlear efferents in some bat species, rats and guinea pigs

    J. Comp. Neurol.

    (1987)
  • A. Aschoff et al.

    Distribution of cochlear efferents and olivo-collicular neurons in the brainstem of rat and guinea pig: A double labeling study with fluorescent tracers

    Exp. Brain Res.

    (1988)
  • A. Aschoff et al.

    Origin of cochlea efferents in some gerbil species

    Exp. Brain Res.

    (1988)
  • T.E. Benson et al.

    Synapses formed by olivocochlear axon branches in the mouse cochlear nucleus

    J. Comp. Neurol.

    (1990)
  • M.C. Brown

    Morphology of labeled efferent fibers in the guinea pig cochlea

    J. Comp. Neurol.

    (1987)
  • M.C. Brown et al.

    Cochlear-nucleus branches of thick (medial) olivocochlear fibers in the mouse: A cochleotopic projection

    J. Comp. Neurol.

    (1991)
  • R. Cantos et al.

    The auditory receptor of the epileptic hamster strain GPG/Vall

    Soc. Neurosci. Abstr.

    (1996)
  • J.H. Dewson

    Efferent olivocochlear bundle: Some relationships to stimulus discrimination in noise

    J. Neurophysiol.

    (1968)
  • P. Fuchs

    The synaptic physiology of cochlear hair cells

    Audiol. Neurootol.

    (2002)
  • Cited by (21)

    • Morphofunctional alterations in the olivocochlear efferent system of the genetic audiogenic seizure-prone hamster GASH:Sal

      2017, Epilepsy and Behavior
      Citation Excerpt :

      We also obtained a distribution pattern of olivocochlear neurons at the ipsicontralateral and rostrocaudal levels, in the GASH:Sal and control hamsters, which was similar to that reported in other rodents [21,46–49]. In our material, the total number of olivocochlear neurons in the control and GASH:Sal hamsters was higher than that obtained in our previous study using FG injections into the hamster's cochlea [21]. In fact, our quantification was very similar to that obtained in the mouse [47].

    • Dendrites of medial olivocochlear neurons in mouse

      2008, Neuroscience
      Citation Excerpt :

      Secondly in favor of an MOC designation, DPO neurons occur on both sides of the brainstem, with the majority on the opposite side (Fig. 3B). This pattern is like other MOC neurons and unlike the mainly ipsilateral LOC neurons, in particular, the shell neurons that are mostly on the same side of the brain as the innervated cochlea (Vetter and Mugnaini, 1992; Azeredo et al., 1999; Sánchez-González et al., 2003). DPO neuron axons in our material were observed to be as thick in diameter as VNTB axons.

    • Efferent System

      2008, The Senses: A Comprehensive Reference
    View all citing articles on Scopus
    View full text