New Insights into the Signal Transmission from Taste Cells to Gustatory Nerve Fibers

Abstract

Taste receptor cells detect chemical compounds in the oral cavity and transfer their messages to gustatory afferent nerve fibers. Considering the coding of taste information, the sensitivity of taste cells and the connection between taste cells and gustatory fibers may be critical in this process. Broadly tuned taste cells and random connections between taste cells and fibers would produce gustatory fibers that have broad sensitivity to multiple taste qualities. Narrowly tuned taste cells and selective connections would yield gustatory nerve fibers that respond to specific taste quality. This review summarizes results showing molecular and morphological aspects of taste bud cells, physiological responses of taste cells, possible connections between taste cells and gustatory fibers, and transmitter release from taste cells, and discusses how taste qualities are encoded among taste bud cells and how taste information is transmitted from taste cells to gustatory nerve fibers.

Introduction

Sensory information of taste is crucial for evaluating nutritious and poisonous substances in foods. In general, sweet, salty, umami, sour, and bitter are considered to be basic taste qualities. Each of these may be responsible for the detection of nutritious and poisonous contents; sweet for carbohydrate sources of calories, salty for minerals, umami for protein and amino acid content, sour for ripeness of fruits and spoiled foods, and bitter for harmful compounds. The detection of these taste qualities begins with the taste receptors on the apical membrane of taste receptor cells. Activation of taste receptor cells leads to depolarization of the taste receptor cell membrane, transmitter release, and activation of gustatory afferent nerve fibers. At this peripheral stage, how do taste receptor cells encode taste qualities and how do they transfer their signals to gustatory nerve fibers?

Recent studies identified molecular mechanisms for reception and transduction of sweet, bitter, umami, and sour taste (Chandrashekar et al., 2006, Roper, 2007). Each of these receptors is expressed in separate population of taste bud cells and genetic elimination of taste receptor (or receptor cells) leads to total loss of sensitivity to a specific taste quality (Adler et al., 2000, Huang et al., 2006, Nelson et al., 2001, Zhao et al., 2003), suggesting that different taste bud cells define the different taste modalities and that activation of a single type of taste receptor cells is sufficient to encode taste quality, supporting “labeled line model” (Chandrashekar et al., 2006). In this case, taste receptor cells respond to a single taste quality and are innervated selectively by gustatory afferent fibers; thereby each gustatory fiber (called “specialist”) may transmit specific taste information to the brain (Frank et al., 2008). Actually, a huge number of fibers in the mammalian gustatory nerve respond to specific taste quality (Frank, 1973, Hellekant and Ninomiya, 1991, Hellekant et al., 1988, Ninomiya et al., 1982, Ninomiya et al., 1984). In addition, taste bud cells that specifically respond to single taste quality are found in mouse (Caicedo et al., 2002, Yoshida et al., 2006a).

But this model might not account for the existence of taste cells and gustatory nerve fibers that are tuned to multiple taste qualities (Caicedo et al., 2002, Frank, 1973, Hellekant and Ninomiya, 1991, Hellekant et al., 1988, Ninomiya et al., 1982, Ninomiya et al., 1984, Yoshida et al., 2006a). To broaden the sensitivity of taste cells, individual taste cells would express different sets of taste receptor or taste bud cells would communicate with each other (Roper, 2006). To broaden the sensitivity of gustatory nerve fibers, individual gustatory fibers would integrate taste information derived from multiple types of taste cells or receive inputs from taste cells that are sensitive to multiple taste qualities.

To transfer taste signals, taste bud cells would release transmitters onto gustatory nerve fibers. Several transmitters have been proposed as candidates: serotonin (5-HT), glutamate, acetylcholine, neuropeptide Y, GABA, and adenosine triphosphate (ATP). Among them, release of ATP and 5-HT is well studied (Finger et al., 2005, Huang et al., 2005, Huang et al., 2007, Romanov et al., 2007) and is probably facilitated by action potentials in taste cells (Vandenbeuch and Kinnamon, 2009). Various studies have demonstrated that taste bud cells generate action potentials in response to taste stimuli (Avenet and Lindemann, 1991, Béhé et al., 1990, Cummings et al., 1993, Furue and Yoshii, 1997, Gilbertson et al., 1992, Yoshida et al., 2006a), indicating that these cells transmit taste information to gustatory nerve fibers. However, only a subset of taste cells has conventional synaptic structures, raising the possibility that some nonsynaptic communications may occur between taste cells and gustatory nerve fibers.

To understand signal transduction from taste cells to gustatory nerve fibers, we first review molecular and morphological aspects of taste bud cells. These features may be closely related to physiological properties of taste bud cells because expression patterns of taste receptors may determine response characteristics of taste cells. Next, we summarize recent results on physiological responses of mouse taste cells and discuss how taste qualities are encoded among taste bud cells. Especially, the relationship between cell types and response properties of taste cells will be illustrated. We also discuss the similarity and difference between taste bud cells in the posterior and anterior parts of tongue. Then, we discuss the possible connection between taste cells and gustatory nerve fibers. Presently, there is no direct evidence showing selective or specific connection between taste cells and gustatory fibers. But comparison of responsiveness of taste cells and gustatory fibers and nerve regeneration experiments might give insights on this problem. Finally we review and discuss transmitter release from taste cells, especially ATP release from taste cells.