Superficial stellate cells of the dorsal cochlear nucleus

Abstract

The dorsal cochlear nucleus (DCN) integrates auditory and multisensory signals at the earliest levels of auditory processing. Proposed roles for this region include sound localization in the vertical plane, head orientation to sounds of interest, and suppression of sensitivity to expected sounds. Auditory and non-auditory information streams to the DCN are refined by a remarkably complex array of inhibitory and excitatory interneurons, and the role of each cell type is gaining increasing attention. One inhibitory neuron that has been poorly appreciated to date is the superficial stellate cell. Here we review previous studies and describe new results that reveal the surprisingly rich interactions that this tiny interneuron has with its neighbors, interactions which enable it to respond to both multisensory and auditory afferents.

Keywords: auditory pathways; electrical synapses; gap junctions; glycine; interneurons.

Figure 1

General circuit diagram of the DCN, divided into three computational domains The auditory domain comprises the auditory input to fusiform cell basal dendrites, and its modification by vertical and D-stellate interneurons. The non-auditory domain receives mossy fiber input to granule cells, and is modified by Golgi and unipolar brush cells. The molecular layer domain comprises the parallel fiber input from granule cells, terminating on fusiform cell apical dendrites and onto cartwheel and SSC cells, both of which in turn control fusiform activity. Omitted here are the giant cells, whose local synaptic circuitry is not well understood.

Figure 2

Distribution of glycinergic neurons in the cochlear nucleus as revealed by GFP labeling in a GlyT2-GFP mouse The image was produced from tiled images captured at a single focal plane with a 20x objective. Cells identified as SSCs (arrows in inset) were small bright cells located in the DCN molecular layer. Cells used for recordings were most often those closest to the edge of the brain stem at the ependymal layer. Cb: cerebellum; DCN: dorsal cochlear nucleus; Md: medulla; VCN: ventral cochlear nucleus. Inset: D: deep layer; F: fusiform cell layer; M: molecular layer.

Figure 3

Response properties of SSCs. (A) Responses to current injections to three different levels illustrating a regular firing pattern. Note that in the middle panel spikelets (shown in insets) were apparent between the full-amplitude spikes. (B) When depolarized from more negative membrane potentials, SSCs generated spike bursts or exhibited an adapting profile of spiking. (C) Example of spontaneous spike activity that was apparent in about half of recorded SSCs. (D) Broad frequency distribution of spontaneous spiking in a population of 29 SSCs.

Figure 4

Gap junctions couple SSCs and fusiform cells. (A) Coupling between a recorded SSC and fusiform pair was tested by injection of hyperpolarizing currents in one cell and then the other, as indicated. Hyperpolarizations of smaller amplitude in the postjunctional cell was taken as evidence of coupling. (B) A similar experiment was performed in a Cx36 knockout mouse, and showed no evidence of coupling. (C) Average coupling coefficients reveal bias for transmission from fusiform cell to SSC. This coupling was present in mice up to 9 weeks postnatal. Data adapted from Apostolides and Trussell (2013b).

Figure 5

Proposed circuit diagram for inhibitory inputs to fusiform cells and the gap junction connectivity (represented by resistors) between SSCs and fusiform cells. SSCs, cartwheel and tuberculoventral cells occupy distinct domains of the fusiform somatodendritic space. SSCs are unique among the three inhibitory cell types in their additional electrical connectivity with fusiform cells and with one another.

Figure 6

Stellate membrane potential modulates fusiform spontaneous spike rate. (A) In an electrically coupled cell pair, injection of hyperpolarizing current steps into the SSC shifted the SSC potential up to 20 mV negative to the resting potential of −65 mV and had a clear inhibitory effect on fusiform spontaneous spiking. (B) Average data from 5 cell pairs shows a near linear dependence of fusiform cell spike rate on SSC membrane potential. Firing rates varied widely among fusiform cells and so were normalized in each cell to the rate during the baseline condition where no hyperpolarizing current step was injected into the stellate cell.