Review
Taste buds as peripheral chemosensory processors

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Abstract

Taste buds are peripheral chemosensory organs situated in the oral cavity. Each taste bud consists of a community of 50–100 cells that interact synaptically during gustatory stimulation. At least three distinct cell types are found in mammalian taste buds – Type I cells, Receptor (Type II) cells, and Presynaptic (Type III) cells. Type I cells appear to be glial-like cells. Receptor cells express G protein-coupled taste receptors for sweet, bitter, or umami compounds. Presynaptic cells transduce acid stimuli (sour taste). Cells that sense salt (NaCl) taste have not yet been confidently identified in terms of these cell types. During gustatory stimulation, taste bud cells secrete synaptic, autocrine, and paracrine transmitters. These transmitters include ATP, acetylcholine (ACh), serotonin (5-HT), norepinephrine (NE), and GABA. Glutamate is an efferent transmitter that stimulates Presynaptic cells to release 5-HT. This chapter discusses these transmitters, which cells release them, the postsynaptic targets for the transmitters, and how cell–cell communication shapes taste bud signaling via these transmitters.

Highlights

► ATP as an excitatory sensory transmitter in taste buds. ► Role of ATP, ACh, adenosine, 5-HT, GABA, and glutamate as taste transmitters. ► Autocrine–paracrine signaling in the taste bud. ► Positive feedback for ATP release from taste buds via P2X and P2Y purinoceptors.

Introduction

As few as three decades ago, taste buds were merely considered inactive interfaces between flavorsome chemicals in the oral cavity and interpretive centers in the nervous system. These peripheral sensory organs were believed to passively convert gustatory stimuli into signals that sensory afferent fibers could propagate to the brain. The cytology of taste buds indicated that their constituent cell population was not homogeneous, but it was not known whether different cells responded to different tastants (e.g., sweet, bitter, etc. compounds), whether there were supporting versus sensory cells, or what transmitter(s) was/were released onto sensory afferent fibers. The intervening years have clarified many of these issues, principally through the efforts of researchers who have applied modern techniques to record functional activity in individual taste cells and who have used molecular biological methodology to identify the proteins found in specific taste bud cells. As a result of these efforts, we now have a tremendously expanded view of the distinct types of cells present in taste buds, how some of these cells contribute to taste reception, what proteins transduce different taste stimuli, and what neurotransmitters are released during taste stimulation. Most importantly, we now understand that the taste bud is a community of interacting cells with significant cell–cell communication taking place during gustatory excitation. Taste buds are no longer thought of as passive sensory structures.

This review tackles the following questions: what interactions take place within the taste bud during taste reception, what are the transmitters involved in these interactions, and how do these interactions shape the signal output from taste buds? I will review the evidence that taste bud cells release ATP, serotonin, norepinephrine, acetylcholine, and GABA to mediate feed-forward and feedback signaling, including excitation and inhibition. Presently, the functional consequences of the cell–cell interactions for taste detection and discrimination are not yet known, but I will hazard some predictions that might be the subject of future studies.

Section snippets

Anatomy of taste buds

There are between 2000 and 5000 taste buds in the human oral cavity, distributed on the tongue, the palate, and to a lesser extent the epiglottis, pharynx, and larynx [1], [2], [3]. There may be important differences between taste buds in different regions on the tongue and elsewhere, although histologically they appear quite similar. Taste buds on the anterior tongue are embedded in fungiform papilla. These taste buds are innervated by the chorda tympani nerve, a branch of the large facial

Physiology of taste buds

Many of the details of taste transduction have been illuminated in the past two decades, in large part through the use of genetically engineered mice, molecular biological studies, patch-clamp recordings, and functional imaging studies. G protein-coupled receptors for sweet, bitter and umami tastants have been identified. Sweet and umami tastants are detected by GPCRs from the small family of Tas1R genes (T1R proteins), and likely other genes as well [26], [27], [28], [29]. Specifically, sugars

Cell–cell communication and taste reception

The thesis of this review is that taste stimulation activates a series of highly orchestrated cell–cell interactions in the taste bud that modulate and shape the signal output from taste buds. The precise significance of the signal modulation is still under investigation and how these cell–cell interactions contribute to taste detection and taste discrimination is yet unknown. Nonetheless, there is no doubt that a certain degree of signal processing takes place in the peripheral sensory organs

Summary and conclusions

This review has focused on the events that occur after taste stimuli have excited taste bud sensory cells, namely the release of taste transmitters. Sweet, bitter, and umami stimulation elicits release of ATP, perhaps as the primary, fast-acting excitatory synaptic transmitter. Knockout studies using mice lacking certain P2X purinoreceptors do not unambiguously identify ATP as the transmitter because synaptic release as a whole is defective in the taste buds of these mice. Instead, the knockout

Acknowledgments

This research has been supported by grants from the National Institutes of Health, National Institute on Deafness and Other Communication Disorders (5R01DC000374 and 1R01DC007630). I wish to thank Nirupa Chaudhari for fruitful discussions and productive collaboration on all the studies described in this report.

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