Synaptic communication and signal processing among sensory cells in taste buds

Abstract

Taste buds (sensory structures embedded in oral epithelium) show a remarkable diversity of transmitters synthesized and secreted locally. The known transmitters accumulate in a cell type selective manner, with 5-HT and noradrenaline being limited to presynaptic cells, GABA being synthesized in both presynaptic and glial-like cells, and acetylcholine and ATP used for signalling by receptor cells. Each of these transmitters participates in local negative or positive feedback circuits that target particular cell types. Overall, the role of ATP is the best elucidated. ATP serves as a principal afferent transmitter, and also is the key trigger for autocrine positive feedback and paracrine circuits that result in potentiation (via adenosine) or inhibition (via GABA or 5-HT). While many of the cellular receptors and mechanisms for these circuits are known, their impact on sensory detection and perception remains to be elaborated in most instances. This brief review examines what is known, and some of the open questions and controversies surrounding the transmitters and circuits of the taste periphery.

Figure 1. The three principal constituent cell types in taste buds

A, confocal micrograph of a taste bud from a Plcb2-GFP mouse. Receptor (type II) cells express GFP (but here, are pseudo-coloured yellow) while presynaptic (type III) cells, immunostained for aromatic amino acid decarboxylase, a 5-HT-synthesizing enzyme, appear green. The dark spaces between the labelled cells are occupied by glial-like (type I) cells that ensheath all the other cells, but are not visualized here. The taste bud resides in oral epithelium (dashed lines). Adapted with permission from J Neurosci (DeFazio, Dvoryanchikov et al. 2006). B, same taste bud, schematized to demonstrate receptor and presynaptic cells in close proximity. The taste bud has a dotted outline while the epithelium is indicated by a dashed outline.

Figure 2. Schematic of the three principal taste cell types and associated transmitters

Cell types are depicted in the same colour scheme as in Fig.1. The transmitters secreted from each cell type are indicated in the corresponding colour. Solid arrows indicate the source and target of each transmitter according to published experimental evidence. For instance, ATP (yellow) from receptor cells activates afferent fibres. Receptor cells also secrete ACh, while ado is generated extracellularly from secreted ATP. Both ACh and ado act on receptor cells. Where direct evidence is lacking, plausible targets are indicated by dashed arrows. For example, GABA accumulates in both type I and III cells; its action on afferent fibres is unreported to date. One transmitter, glu, is secreted from nerve terminals and acts on presynaptic cells as discussed in the text. ACh, acetylcholine; ado, adenosine; glu, glutamate.