Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus

Abstract

We distinguish two types of large multipolar cells designated sustained (CS) and onset (OC) choppers in the anterior posteroventral cochlear nucleus (A-PVCN)/nerve root region on the basis of certain anatomical and physiological features. CS axons head into the trapezoid body, while OC axons use the intermediate acoustic stria of Held. At the electron microscopic (EM) level, collateral terminals of OC axons contain pleomorphic vesicles; CS terminals contain small round vesicles. CS dendritic trees tend to be distributed in a stellate fashion while OC dendritic trees tend to be elongated. At the EM level the sustained chopper somata are sparsely innervated while the proximal dendritic tree receives considerably more input. The OC somata are highly innervated and this heavy innervation continues out onto the proximal dendrites. Distally the dendritic innervation falls off considerably for both categories. Physiologically, members of the OC population have wider dynamic ranges at the characteristic frequency (CF), wider response areas that are typically not flanked by inhibitory sidebands, and responses to short tones that do not show the same form of regularity expressed by sustained choppers. Intracellularly the sustained choppers exhibit sustained depolarization to short tones for the duration of the stimulus with resultant regular spiking at a rate that is stimulus level dependent. The response to swept tone shows this same level-dependent regularity. In response to tones, the OC cells also show a sustained depolarization whose amplitude is stimulus-level dependent but whose range is much greater and whose onset is initiated more abruptly. Although the onset component of the OC spike output is reliably initiated by these levels of depolarization, regular firing to the sustained depolarization is not initiated at levels of depolarization that would surely generate regular firing in sustained choppers. This regularity is also absent in the swept tone response despite marked levels of excitation.

Onset Neurones in the Anteroventral Cochlear Nucleus Project to the Dorsal Cochlear Nucleus

“…The functional role of this local inhibition can be inferred only indirectly, but there has been a proposal that broadly tuned On-C cells inhibit narrowly tuned chopper cells (Smith and Rhode 1989). There is also evidence from in vitro work that large D-type stellate cells inhibit the smaller T stellate cells.…”

“…These onset cells integrate inputs from auditory nerve fibers with a broad range of BFs , acting as coincidence detectors with a relatively narrow coincidence window ; they respond better to broadband signals than to pure tones; and they exhibit relatively wide dynamic ranges (Smith and Rhode 1986;Winter and Palmer 1995). Physiologically characterized, VCN onset cells have been found to exhibit large multipolar morphology (Smith and Rhode 1989), and VCN cells with this morphology have been found to be glycinergic (Doucet et al 1999) and are thought to provide inhibition of other neurones in the cochlear nucleus such as the T stellate cells (Ferragamo et al 1998). …”

“…Bushy cells provide more-or-less faithful transmission of auditory nerve firing patterns (Pfeiffer 1966) and project this information into pathways for comparison of the activity from the two ears to extract cues for localizing sounds. Stellate cells have more diverse physiological properties, producing a variety of onset or choppingtype responses (Young et al 1988;Blackburn and Sachs 1989;Smith and Rhode 1989;Winter and Palmer 1990).…”

“…Some of the criteria are purely structural while others are functional, but there seems to be a good correspondence between them. The first class has variously been termed type I (sparse synapses formed on the soma) (Cant 1981), small planar or marginal cells (Doucet and Ryugo 1997), type T (axon projecting into the trapezoid body) (Oertel et al 1990), glycine negative (Alibardi 1998(Alibardi , 2001, and cells with chopping responses (Smith and Rhode 1989). The second class has been termed type II (dense covering of synapses on the soma), large radiate cells, type D (dorsal projecting axons), glycine positive, and cells with onset responses (by the same authors).…”

Vesicular Glutamate Transporter 2 Is Associated with the Cochlear Nucleus Commissural Pathway

“…CN-commissural projections terminate in most regions of the CN including the granule cell domain (GCD), which includes the external shell of the ventral CN (VCN) and the fusiform cell layer of the dorsal CN (DCN) (Schofield and Cant 1996;Weedman et al 1996;Zhou et al 2007). A common assumption over the past two decades has been that the majority of CN-commissural projections arise from the broadly tuned, inhibitory, D stellate or type II multipolar cells (Cant and Benson 2003;Doucet and Ryugo 2006;Smith et al 2005;Smith and Rhode 1989). However, recent observations (Doucet et al 2009) suggest that this pathway is composed of at least two populations of cells: large multipolar cells that resemble the glycinergic, D stellate cells, as well as small-and medium-sized multipolar cells that account for approximately 60% of CNcommissural neurons.…”