Introduction to the superior olivary complex

The superior olivary complex (SOC), a group of interrelated nuclei bilaterally located in the basal brainstem, is part of the mammalian central auditory system consisting of various neural sites connected to each other by multiple parallel pathways in which many projections are tonotopically organized. The functions of the SOC include the processing of cochlear signals via the ascending auditory pathway, the detection of interaural sound intensity and time differences as the basis of spatial mapping, as well as feedback control of cochlear mechanisms (see Moore, 1994; Tsuchitani and Johnson, 1991; Warr, 1992). Although the SOC is also involved in non-auditory functions, and some auditory information bypasses the SOC, there is no doubt that it plays a pivotal role in hearing processes. A wide range of techniques have been employed to unveil these functions, ranging from single-unit electrophysiology to recording of the auditory brainstem response, from histochemistry to in situ hybridization, and from neuronal tracing to lesions and the production of hearing traumata. In the present volume of Microscopy Research and Technique, several groups investigating the SOC survey their results and highlight recent advances in the field. The cells responsible for the perception of sound are the inner and outer hair cells (IHC, OHC) of the organ of Corti in the cochlea. They are arranged parallel to the longitudinal axis of the cochlear duct. Both types of sensory cells are contacted by afferent dendrites from spiral ganglion neurons. Hair cell information is, thus, transmitted to the cochlear nucleus (CN) complex where spiral axons terminate. They branch to make synaptic contacts in the anterior and posterior ventral and in the dorsal CN. The CN of both sides project to the SOC, which is composed of three principal nuclei, i.e., the lateral and medial superior olivary nuclei (LSO, MSO) and the medial nucleus of the trapezoid body (MNTB) and of some less-defined periolivary neuronal groups. The location of the SOC in the guinea pig brainstem is shown in Figure 1. The comparative study of the SOC in many mammals revealed that considerable differences between species exist in morphology, extent, and function of the nuclei (for review see Schwartz, 1992). For example, the periolivary groups and, in particular, the MSO (usually associated with processing of interaural time differences) are prominent in the human SOC (see Moore et al., 1999; Moore, pages 403–412 this issue). The superior olivary complex sends, via the lateral lemniscus, ascending axons to the nuclei of the lateral lemniscus (NLL) and to the subdivisions of the inferior colliculus (IC), the target of virtually all parts of the ascending auditory pathway (for overviews see Aitkin, 1989; Webster, 1995). The anatomical patterns and roles of the ascending projections have been reviewed previously (Helfert et al., 1991). There is evidence that the ipsilateral MSO and contralateral LSO projections to the central nucleus of the IC are excitatory, while those from the ipsilateral LSO are inhibitory (Oliver et al., 1995). The modes through which SOC information is integrated with those from CN and NLL to regulate processing in the IC are important for auditory functions such as hearing and sound localization. The routes involved and their functional roles are discussed by Oliver in this issue (pages 355–363). The major ascending pathway then connects the IC to the medial geniculate body (MGB) and, in turn, with the primary auditory cortical complex. In the human brain, the auditory cortex is located in the transverse gyri of Heschl (areas 41 and 42 of Brodmann). In addition to its ascending projections, the SOC also exhibits a descending projection directed to the cochlea. Axons of SOC neurons build the so-called olivo-cochlear bundle (Papez, 1930; Rasmussen, 1946) and make direct synapses with OHC or synapse at afferent processes of spiral ganglion cells at the base of IHC. In the rat, a predominantly ipsilateral projection stems from small neurons with polar dendrites in the lateral SOC. The other group is located in the medial SOC and consists of larger multipolar neurons that project mainly to the contralateral cochlea (White and Warr, 1983). The organization of the descending auditory systems and, in particular, of olivo-cochlear projections have been comparatively described in detail (Spangler and Warr, 1991; Warr, 1992). Some recently discovered aspects of the descending projections are mentioned in this issue (Reuss and Riemann, pages 318–329; Robertson and Mulders, pages 307–317). In addition, there is evidence that a small, third group of neurons exists that provides both ascending and descending projections. This was found upon double retrograde neuronal tracing following injection of different tracer substances into the IC and the ipsilateral cochlea (Reuss et al., 1999; Riemann and Reuss, 1998). The neuroactive substances found in SOC neurons include acetylcholine, amino acid transmitters such as glutamate (Moore and Moore, 1987), glycine (Bledsoe et al., 1990), GABA (Wynne et al., 1995), and various neuroactive peptides. Cholecystokinin, somatostatin, substance P, and enkephalins were detected in afferent fibers (which is also the case for serotonin and noradrenaline). Their sources and possible functional roles were reviewed previously (Caspary and Finlayson, 1991; Wenthold, 1991) and are discussed here (Robertson and Mulders, this issue, pages 307–317). Found in neurons were calcitonin gene-related peptide, enkephalins and dynorphins, which may co-exist in SOC neurons (Safieddine and Eybalin, 1992). Some of these cells were related to the olivo-cochlear projections that comprise medial and lateral systems (MOC, LOC). They have various functions including frequency selectivity, augmentation of signal-to-noise ratio and protection of the cochlea from sound damage, probably by suppressing cochlear sensitivity utilizing contractile responses of OHC (see Warr, 1992). The set of neuroMICROSCOPY RESEARCH AND TECHNIQUE 51:303–306 (2000)