Cracking taste codes by tapping into sensory neuron impulse traffic
Introduction
Taste identifies nutritious and poisonous substances. This review focuses primarily on what is known about the way in which mammalian peripheral taste neurons encode information about taste quality (Nowlis and Frank, 1981); we also comment on preference (valence); both qualities and preferences vary in intensity. Encoding begins with molecular taste receptors (TR) in plasma membranes of taste-bud receptor cells (TRC), which activate afferent neurons that signal qualitative differences among a large and chemically diverse set of compounds. Many can be condensed into a limited number of perceptually similar categories once oral sensations derived from olfactory and trigeminal receptors, which contribute to overall sensory experience and influence decisions to ingest or reject stimuli, are excluded. Sugars, salts, acids and bitter substances form the four taste categories most frequently used as standard stimuli in scientific investigations of taste in humans and other mammalian species. It is likely no coincidence that corresponding perceptual categories of sweet, salty, sour, and bitter are intrinsically related to naturally consumed major nutrient groups (e.g., carbohydrates and salts) and harmful substances (e.g., toxins and acids) avoided by mammals and other vertebrates.
Elemental components of other important nutrients, protein and fat, are free amino acids and fatty acids, respectively, which enhance palatability of food and stimulate consumption. For example, glutamate, a free amino acid found in many foods, meat and fish included, may be added to enhance the flavor of a cuisine. The unusual taste quality elicited by l-glutamate is described as “savory,” commonly called “umami” from the Japanese (Yamamoto et al., 1988, Yamamoto et al., 1991, Hettinger et al., 1996, Galindo-Cuspinera and Breslin, 2006, McCabe and Rolls, 2007). Also, lingual lipase is present in the oral cavity to rapidly break down fats into free fatty acids, possibly the critical agents for eliciting a fat “taste” (McCormack et al., 2006). Umami taste is increasingly included on the list of taste categories, as is fat, although to a far lesser extent. Despite their ability to enhance palatability, the inclusion of umami and fat as taste categories remains controversial. Yet there has long been general agreement on sweet, salty, sour and bitter as unique human taste experiences (McBurney and Gent, 1979) and this perspective has strongly influenced research in other species.
Taste activation by nutritious and poisonous substances has a powerful influence on physiology and behavior. Taste stimuli trigger changes in autonomic and endocrine activity, and elicit somato-motor reflexes that foster or terminate consumption. For example, besides taste sensations, taste stimuli elicit salivation (Bradley et al., 2005) and cephalic insulin release (Teff, 2000) to assist digestion, or oral-motor ejection reflexes to prevent swallowing of toxins, a primary province of CN IX afferents in rats (King et al., 2000). And, stimulation of pharyngeal and laryngeal taste buds activate CN X afferent limbs of protective reflexes (Bradley, 2000). Factors like physiological state and stimulus context have substantial impact on the strength of signals transmitted by peripheral taste nerves (Contreras and Frank, 1979, Formaker et al., 1997). Apparently, in real life, sodium salt and sugar tasting are regulated by need for Na+ and an uncontaminated carbohydrate source.
The rodents: rat, hamster and mouse, the foremost research models for taste and its effects on ingestion, and new and old world primates, including humans, have provided critical knowledge about taste coding mechanisms. Much of this knowledge comes from parallel studies using electrophysiological recording of whole nerve and single-neuron responses and psychophysical studies of taste-mediated behavior. We will draw heavily upon the literature using this two-barreled approach to address peripheral coding mechanisms of taste. In mammals, the chorda tympani (CT) branch of cranial nerve (CN) VII innervates taste buds in fungiform papillae distributed across the anterior tongue, the greater superficial petrosal (GSP) branch of CN VII innervates palatal taste buds, and the lingual branch of the glossopharyngeal (GL), CN IX, innervates taste buds in foliate papillae of the posterior-lateral and circumvallate papillae of the posterior-medial tongue. Rat CN IX and CN VII overlap in the anterior clefts of the foliate papillae (Miller et al., 1978). Much of the experimental literature on peripheral taste coding arises from work involving the CT nerve and its geniculate ganglion. This review, therefore, reflects that emphasis. Humans appreciate all taste qualities when stimuli are applied to either anterior or posterior tongue regions (Grover and Frank, 2008); however rats without taste information transmitted by CN VII fail to discriminate taste-stimulus quality (Spector and Grill, 1992). Information transmitted by the rat CT also supports mouth “gapes” attributed to learned sucrose aversions (Eylam et al., 2000); and, after rewiring the CT to GL receptive fields (King et al., 2008), information supporting aversive reflexes primarily transmitted by the normally wired lingual branch of CN IX (King et al., 2000). A similar conversion shown for sensory function with rewiring in rats and mice was interpreted as a possible selective coupling between afferent and peripheral target (Oakley, 1967, Ninomiya, 1998) that would be useful for maintaining consistent information transmission during normal TRC turnover.
Although taste qualities distinguished by people (McBurney and Gent, 1979) strongly influenced interpretations of classical taste nerve recordings, the first recordings also anticipated the distinctive taste worlds of different species (Anderson et al., 1950, Beidler et al., 1955, Pfaffmann, 1955), nations reflecting their individual genomes (Shi et al., 2003, Shi and Zhang, 2006). However, they did not anticipate discovery of distinct sets of species-dependent TR that had stimulus chemistries consistent with discrete sweet, glutamate, bitter and sour taste qualities (Chandrashekar et al., 2006). Interpretation of the 21st century findings in the context of characteristics of CT neuron types, discovered electrophysiologically, concludes this review.
Section snippets
Classic recordings and the coding controversy
When it first became possible to “tap in on the electrical impulse traffic in the sensory nerves” (Pfaffmann, 1984), the function of an individual mammalian taste neuron was a puzzle. Electrophysiological recordings from taste nerves of cats, dogs, domestic rabbits, lab rats and golden hamsters did not reveal four functional classes of single-nerve fibers, one for each of the four taste qualities expected from human taste sensation; i.e., four “labeled lines.” Single- and few-fiber preparations
Best-stimulus-behavior consonance
The golden hamster (Mesocricetus auratus) is a valuable alternate to the ubiquitous laboratory rat as a rodent model for taste studies because the hamster CT responds more equally to sucrose, quinine·HCl, NaCl and HCl. The rat CT responds well only to the ionic stimulus prototypes: those representing the human salty and sour qualities, and less well to sweet and bitter stimuli (Beidler et al., 1955, Lundy and Contreras, 1999, Breza et al., 2006, Breza et al., 2007). Outbred lab golden hamsters,
Species and inbred strains differ in what they can taste
It is increasingly clear that there are profound species differences in taste stimulus chemistry. Knowledge of a species ecological niche, that is, what the species has available to sample and decide whether or not to eat or drink, is needed to understand what a species must code as tastes. A model developed by Boudreau more than 20 years ago has facial nerve (CN VII) systems composed of four distinct stimulus detectors (modules or qualities); however, a given species, be it rat, cat, goat or
Contexts, needs and experiences matter
Gustatory coding is dynamic, capable of detecting transient changes in a chemical milieu. Taste stimuli in food and drink are introduced into a complex oral chemical context and tastes are perceived transiently above an ambient salinity (Bartoshuk, 1974). A constant component in the oral environment is saliva, which is itself a variable formulation (Schneyer et al., 1972); and single-stimulus, self-adaptation, or multiple stimulus, cross-adaptation, control our perceptual experiences.
Taste quality codes
Unexpected non-specificity in the very first taste nerve recordings led to the idea that “across fiber patterns” may exclusively code taste qualities (Pfaffmann, 1941), a concept that persevered in spite of many, subsequent neural recordings demonstrating species-dependent specificity that matched behavioral simplicity (e.g., Hellekant et al., 1997a, Ninomiya and Funakoshi, 1988, Contreras and Lundy, 2000, Frank, 2000). With discovery and characterization of TRs with powerful genetic techniques
Acknowledgements
This review, supported by NIH NIDCD grants DC004099 and DC004849 (MEF), DC004785 (RJC), and DC006698 (RFL), is dedicated to the memory of Y. Zotterman, C. Pfaffmann and L.M. Beidler, who founded taste-nerve electrophysiology while establishing a multidisciplinary chemosensory specialty. We acknowledge the Pfaffmann memoir (1984) for inspiring the title and two anonymous reviewers for their insights, which are incorporated into this review.
Glossary
- Adaptation
- Adaptation is a decrease in response while continuously presenting a stimulus. Cross adaptation is a decrease in response to stimulus B after stimulus A has been presented.
- E neuron
- An E neuron is a CT nerve-fiber or GG cell with an electrolyte-sensitive (also called acid-best) response profile, an electrolyte generalist.
- Generalist
- A generalist is a neuron that responds to stimuli with distinctly different taste qualities.
- N neuron
- An N neuron is a CT nerve-fiber or GG cell with an
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