Elsevier

Hearing Research

Volume 172, Issues 1–2, October 2002, Pages 18-36
Hearing Research

Electrophysiological characterization of the superior paraolivary nucleus in the Mongolian gerbil

https://doi.org/10.1016/S0378-5955(02)00353-2Get rights and content

Abstract

The superior paraolivary nucleus (SPN) of the superior olivary complex (SOC) though morphologically well described, has not been characterized physiologically. Here we report the basic response properties of SPN units acquired with extracellular recording techniques under monaural acoustic stimulation in the Mongolian gerbil. Poststimulus-time histograms corresponded to those described earlier for the cat’s cochlear nucleus (onset, chopper, primary-like), and partly to those previously acquired in other SOC nuclei (tonic, off/rebound). Two-thirds of the units responded solely to contralateral stimulation (40% excitatory [E], 19% inhibitory [I], 6% mixed [EI]). Most of the remainder responded equally to stimulation from either ear (18% I.I, 9% E.E). Overall, the monaural contralateral input was more effective than the ipsilateral and bilateral input. Characteristic frequencies and response areas covered the entire hearing range of the gerbil and the units mostly showed broad frequency-tuning. In combination, these properties suggest that the SPN might be a constituent of an afferent pathway encoding stimulus features across broad frequency ranges.

Introduction

The superior paraolivary nucleus (SPN) is a prominent nucleus of the superior olivary complex (SOC) in a number of rodents (Fig. 1) and has been identified as a significant nucleus within ascending and descending auditory pathways. The SPN is considered by many to be homologous to the dorsomedial paraolivary nucleus (DMPO) of guinea pigs, cats and dogs (reviewed by Schofield and Cant, 1991, Colombo et al., 1996, Berrebi et al., 1997, Kelly et al., 1998). The use of retrograde neurotracers has shown that the SPN receives bilateral (predominantly contralateral) input from octopus, multi-polar and globular bushy cells (GBCs) of the ventral cochlear nucleus (VCN; rat: Friauf and Ostwald, 1988, Saldana et al., 1994; gerbil, mouse: Kuwabara et al., 1991; guinea pig: Thompson and Thompson, 1991a, Thompson and Thompson, 1991b, Schofield, 1995), the latter being collaterals of projections to the medial nucleus of the trapezoid body (MNTB; Morest, 1968, Kuwabara et al., 1991). Afferents from octopus and bushy cells are thought to act through excitatory transmitter, since they are immunonegative to both inhibitory transmitters γ-aminobutyric acid (GABA) and glycine (Roberts and Ribak, 1987, Moore and Moore, 1987, Kolston et al., 1992). Other studies suggest that a group of multi-polar neurons, which send their axons through the intermediate acoustic stria (IAS), carry an inhibitory transmitter (Roberts and Ribak, 1987, Friauf and Ostwald, 1988, Smith and Rhode, 1989, Schofield, 1995, see also discussion for this topic).

Tracer studies also provide evidence that the SPN receives an additional input from the ipsilateral MNTB through axons which also form collateral terminations on somata of medial superior olive (MSO) and lateral superior olive (LSO) neurons (Kuwabara and Zook, 1991, Kuwabara and Zook, 1992). This is presumably a glycinergic projection, which gives rise to a dense meshwork of glycinergic fibers and terminals within the SPN (Helfert et al., 1989, Kulesza et al., 1998, Kulesza and Berrebi, 2000). GABAergic fibers and terminals, on the other hand, are only sparsely distributed within the neuropil of the SPN (Roberts and Ribak, 1987, Moore and Moore, 1987, Kulesza and Berrebi, 2000).

Collaterals from projections of the MSO to the ipsilateral inferior colliculus (IC) are another source of a topographically organized input to the SPN (Kuwabara and Zook, 1999), as well as projections from the ventral nucleus of the lateral lemniscus (VNLL) and dorsal nucleus of the lateral lemniscus (DNLL) that descend towards the SOC (cat: Whitley and Henkel, 1984; rat: Bajo et al., 1993).

The SPN itself is a major source of ascending projections to the ipsilateral central nucleus and dorsal cortex of the IC (Fig. 1C; gerbil: Nordeen et al., 1983, Benson and Cant, 2000; rat: Gonzalez-Hernandez et al., 1996). A weaker projection to the contralateral IC has so far only been described in rats (Kelly et al., 1998, Fuentes et al., 1999, Saldana and Berrebi, 2000) and guinea pigs (Schofield, 1991, Schofield and Cant, 1992). The topography of the ipsilateral projection from the SPN to the central nucleus of IC has been shown for the rat (Kelly et al., 1998, Saldana and Berrebi, 2000).

While in the guinea pig a bilateral descending projection from the DMPO/SPN to the cochlea has been described (Robertson, 1985, Tokunaga, 1988, Winter et al., 1989, Thompson and Thompson, 1991b), the SPN of rats and gerbils lacks such descending projections (White and Warr, 1983, Aschoff et al., 1988, Vetter et al., 1993). The cochlear nucleus (CN) of these species does, however, receive ipsilateral and (weaker) contralateral projections from the SPN (gerbils: Kuwabara and Zook, 1994; rats: Colombo et al., 1996; guinea pigs: Winter et al., 1989, Ostapoff et al., 1990, Benson and Potashner, 1990, Ostapoff et al., 1997). A SPN projection to the ipsilateral MNTB has also been described (Kuwabara et al., 1991).

Based on the different shapes of their somata three types of neurons were distinguished in the SPN: multi-polar round, triangular, and elongated spindleform neurons (gerbil: Nordeen et al., 1983; guinea pig: Schofield and Cant, 1991; mice: Ollo and Schwartz, 1979). Schofield and Cant (1991) also showed in the guinea pig that these morphologically distinct neuron types differ in their projections: multi-polar neurons project to the IC, while spindleform neurons project to the CN. In contrast to this, Kulesza and Berrebi (2000) only reported one homogeneous population of multi-polar neurons in the rat SPN.

The SPN neurons have the largest somata of all SOC neurons (Ollo and Schwartz, 1979, Schofield and Cant, 1991), and they form far-reaching dendritic fields, which partly extend beyond the borders of the SPN towards the ventral nucleus of the trapezoid body (VNTB; Morest, 1968, Ollo and Schwartz, 1979, Saldana and Berrebi, 2000, Kulesza and Berrebi, 2000). GABA was identified in most of the large, polygonal neurons and also in a few small, fusiform/oval neurons by immunocytochemistry (guinea pig: Helfert et al., 1989; rat: Kulesza and Berrebi, 2000). Roberts and Ribak (1987) labeled the GABA-synthesizing enzyme glutamic acid decarboxylase (GAD) in a substantial population of medium- to large-sized, oval neurons of the gerbil SPN. Glycine was located in a few large, polygonal and also in small oval or fusiform neurons (guinea pig: Helfert et al., 1989; rat: Kulesza et al., 1998). Thus, most of the projections arising from the SPN seem to be glycinergic and/or GABAergic (GABAergic to IC: Gonzalez-Hernandez et al., 1996; glycinergic to IC: Saint Marie and Baker, 1990; GABAergic and glycinergic to CN: Ostapoff et al., 1990, Ostapoff et al., 1997, Benson and Potashner, 1990).

Despite the breadth of knowledge about the morphology of SPN neurons and their connectivities, we still lack information about their response properties to acoustic stimuli. To date, the little that we know can be classified as ‘additional results’ from electrophysiological investigations which had their main focus on other SOC nuclei or on the SOC as a whole (cat: Guinan et al., 1972a, Guinan et al., 1972b; dog: Goldberg and Brown, 1968; gerbil: Brueckner et al., 1994, Brueckner et al., 1996, Spitzer and Semple, 1995, Kuwada and Batra, 1999). In the present study, the acoustically evoked response properties of SPN units were investigated with extracellular recordings. Ipsi- and contralateral, monaural tone-burst stimulation were used to characterize the units response areas, their frequency selectivity and the time course of the responses. Some of the data contained herein have been presented in abstract form (Dehmel et al., 1999).

Section snippets

Materials and methods

Six Mongolian gerbils (Meriones unguiculatus) were used in this study (age between 2 and 3 months). All experimental procedures were approved by the Saxonian District Government, Leipzig. Animals were anesthetized during surgery and the recording procedure with a xylazine-hydrochloride/ketamine-hydrochloride mixture (Rompun®, Bayer, xylazine 0.5 mg/100 g body wt i.p.; Ketavet®, Upjohn, ketamine 13 mg/100 g body wt i.p. initial dose, one third of the initial dose as supplementary s.c. when

Excitatory and inhibitory discharge patterns

The responses of SPN units evoked by monaural pure tone stimulation of either of the two ears, can be classified as excitatory and/or inhibitory with respect to an increase or decrease of the discharge rates relative to the spontaneous activity (Fig. 2). The units’ temporal response patterns were evaluated from the dot-raster displays and PSTHs (Fig. 3). The percentages of the different response types are listed in Fig. 4 with reference to the respective ipsilateral and contralateral

Discussion

The two most striking features of SPN physiology are the broad frequency-tuning of the neurons and the incidence of afferent inhibitory input. In 32% of the entire unit sample acoustically evoked inhibition is conveyed following stimulation of either the ipsilateral or the contralateral ear (XI or IX, ‘X’ being ‘0’ or ‘E’), and in 18% inhibition is manifested after stimulation of each of the two ears (I.I). Unit types with significant inhibitory input have also been described for the gerbil SPN

Acknowledgements

This work was supported by DFG GRK 250/1-96 and DFG Ru 390-15/1. We thank P. Stevenson and W.R. Lippe for critically reading earlier versions of the manuscript.

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