Elsevier

Hearing Research

Volumes 216–217, June–July 2006, Pages 31-42
Hearing Research

Research paper
Neural timing, inhibition and the nature of stellate cell interaction in the ventral cochlear nucleus

https://doi.org/10.1016/j.heares.2006.01.016Get rights and content

Abstract

The ventral cochlear nucleus (VCN) stellate cell population comprises two clusters: narrowly-tuned, excitatory T stellate neurons, and D stellate neurons, a broadly-tuned population of inhibitory cells. These neurons respond to best frequency (BF) tone bursts in a chopper or onset manner, respectively. Through extensive local and commissural projections the D stellate population provides a source of fast inhibitory input to both intrinsic and contralateral T stellate neurons. Whilst the nature of interactions between intrinsic stellate populations is difficult to examine, our previous intracellular investigations of the commissural pathway have provided a means by which to study this relationship in the in vivo preparation. It is the aim of this paper to both review and extend our understanding of the link between stellate populations and their involvement in the commissural pathway by presenting an overview of the results attained in our recently expanded study. The sample of 17 intracellular and 34 extracellular onset chopper (OC) and late/ideal (OnL/OnI) neurons revealed antidromic activity in 31.4% of neurons following contralateral stimulation, providing physiological evidence that OnL/OnI neurons also contribute projections to the commissural connection. Alternatively, 64.7% of the 34 intracellularly-recorded chopper neurons displayed fast, monosynaptic inhibitory potentials. This commissural input was found to influence the timing of neural activity in chopper neurons, providing insight into the relationship that exists between T and D stellate neurons.

Introduction

The ventral cochlear nucleus (VCN) comprises two populations of stellate/multipolar neuron: T and D stellate. The T stellate neuron, named for the trajectory of its axonal projection into the trapezoid body (Oertel et al., 1990), has also been termed planar due to the orientation of dendrites in line with the plane of incoming auditory nerve fibres (Doucet and Ryugo, 1997), and type I on account of its sparse somatic synaptic coverage (Cant, 1981). The activity recorded from these neurons in response to best-frequency (BF) tone bursts can be described as either sustained or transient chopper (CS and CT, respectively) (Feng et al., 1994, Ostapoff et al., 1994, Palmer et al., 2003, Paolini et al., 2005, Rhode and Smith, 1986, Smith and Rhode, 1989). Alternatively, axonal projections of the D stellate neuron travel dorsally (Oertel et al., 1990). Also named radiate for their dendritic organization (Doucet and Ryugo, 1997), or type II, due to their dense somatic coverage (Cant, 1981), the D stellate neuron responds to BF tones in an onset chopper (OC) or onset-late (OnL) manner (Arnott et al., 2004, Palmer et al., 2003, Paolini and Clark, 1999, Paolini et al., 2005, Rhode and Smith, 1986, Smith and Rhode, 1989, Smith et al., 2005, Winter and Palmer, 1995). These response patterns are noted for their broad tuning and large dynamic range, qualities reflective of the D stellate cells’ far-reaching dendritic branches, and subsequent wide-ranging afferent input. Moreover, this feature affords the OC or OnL neuron with the ability to respond more vigorously to broadband stimuli, such as noise, than pure tones (Winter and Palmer, 1995).

The presence of oval/pleomorphic vesicles within the axon terminals of OC neurons (Smith and Rhode, 1989), together with the identification of glycine immunoreactivity in a population of large multipolar neurons in the VCN (Doucet et al., 1999, Kolston et al., 1992, Peyret et al., 1987, Wenthold et al., 1987), suggests that the D stellate population is glycinergic, and its input therefore inhibitory. The projections of these neurons terminate extensively across both VCN and dorsal cochlear nucleus (DCN) regions (Adams, 1983, Arnott et al., 2004, Doucet and Ryugo, 1997, Doucet et al., 1999, Palmer et al., 2003, Smith and Rhode, 1989, Smith et al., 2005), and have subsequently been implicated as the source of wideband inhibition throughout the cochlear nucleus (CN: Davis and Young, 2000, Doucet et al., 1999, Ferragamo et al., 1998, Joris and Smith, 1998, Nelken and Young, 1994, Winter and Palmer, 1995). Amongst the potential targets of D stellate projections are neurons of the T stellate population (Ferragamo et al., 1998, Smith and Rhode, 1989). This wideband inhibition of T stellate neurons has been proposed as a means of sharpening spectral contrast through suppression of off-BF (lateral) input (Rhode and Greenberg, 1994), or more recently, improve spectral coding via its influence on neural timing (Paolini et al., 2004, Paolini et al., 2005).

Whilst the presence of inhibitory input to T stellate neurons is well documented (Adams, 1993, Altschuler et al., 1986, Babalian et al., 2002, Cant, 1992, Ferragamo et al., 1998, Josephson and Morest, 1998, Juiz et al., 1996, Paolini et al., 2004, Paolini et al., 2005, Saint Marie et al., 1993, Wenthold et al., 1988, Wickesberg and Oertel, 1990, Wu and Oertel, 1986), the nature of D stellate input to T stellate neurons is difficult to attest in the in vivo preparation. Given the weight of evidence implicating D stellate neurons as the source of commissural input (Alibardi, 1998, Arnott et al., 2004, Cant and Gaston, 1982, Davis, 2005, Joris and Smith, 1998, Needham and Paolini, 2003, Schofield and Cant, 1996, Shore et al., 1992, Smith et al., 2005, Wenthold, 1987), and the T stellate population as a target (Alibardi, 2000a, Babalian et al., 1999, Babalian et al., 2002, Needham and Paolini, 2003, Schofield and Cant, 1996, Shore et al., 2003), the manner in which D stellate neurons influence the activity of T stellate neurons, can also be studied through an examination of the commissural projection.

The following results describe the physiological properties of VCN T and D stellate activity as attained through in vivo intracellular recordings, and document the nature of the interaction between the two groups, as observed through investigations of the commissural connection. Whilst the main findings presented have been described in our previous publications (Needham and Paolini, 2003, Paolini and Clark, 1999, Paolini et al., 2004, Paolini et al., 2005), the larger sample of neurons on which we report here is able to provide a greater overview of the commissural connection and stellate cell physiology, serving to both support and extend our understanding of (i) the intracellular response properties of stellate neurons, (ii) the influence of D stellate input on T stellate activity, and (iii) the involvement of stellate populations in the commissural connection.

Section snippets

Preparation

Electrophysiological experiments were performed on 90 adult Hooded-Wistar rats (250–350 g). All procedures were carried out in accordance with the Royal Victorian Eye and Ear Hospital Animal Research Ethics Committee guidelines (projects 95-037-01 and 04-105) and adhered to the guidelines of the National Health and Medical Research Council of Australia. The main components of this protocol have been described previously (Needham and Paolini, 2003, Paolini and Clark, 1999, Paolini et al., 2004,

Results

Intracellular recordings were obtained for 17 onset and 34 chopper neurons. The mean (± standard error (SE)) RMP for all intracellularly recorded neurons was −49.4 ± 1.3 mV, with mean AP amplitude of 36.8 ± 1.5 mV, mean BF of 16.6 ± 1.3 kHz, and mean threshold at BF of 38.2 ± 3.6 dB. The activity of an additional 34 onset neurons was obtained with extracellular recordings: mean BF 19.0 ± 1.4 kHz and mean threshold 47.0 ± 2.8 dB. Of the 85 neurons described here, eight onset neurons (three intracellular; five

Discussion

This study examines the intracellular activity of T and D stellate neurons in the VCN, describing the nature of the interaction between these populations through activation of the commissural pathway. The more extensive overview provided here by our increased sample of stellate neurons is able to both confirm and expand upon the results of our previous studies by illustrating that (i) D stellate neurons of both OC and OnL/OnI response types contribute projections to the commissural connection;

Acknowledgements

The authors thank R.E. Millard for engineering support. Funding provided by a Melbourne Research Scholarship and the Department of Otolaryngology, The University of Melbourne.

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