Taste Has Five Submodalities or Qualities
The primary function of the gustatory system is nutritional. Humans and other mammals can distinguish five different taste qualities: sweet, bitter, salty, sour, and umami, the taste associated with amino acids. Taste chemicals (tastants) perceived as sweet are associated with food high in caloric content, while those sensed as umami are indicative of protein.
Consistent with the nutritional importance of carbohydrates and proteins, both sweet and umami tastants elicit pleasurable sensations in humans and are attractants for animals. In contrast, bitter tastants, which are often found in poisonous plants, elicit an aversive response that is innate in animals as well as human infants and likely prevents the ingestion of toxic substances.
Taste is often thought to be synonymous with flavor. However, taste refers strictly to the five qualities encoded in the gustatory system, whereas flavor, with its rich and varied qualities, actually stems from a combination of inputs from the gustatory, olfactory, and somatosensory systems.
Taste Detection Occurs in Taste Buds
In the gustatory system sensory signals generated in the mouth are relayed through the brain stem and thalamus to the gustatory cortex (Figure 32–13). Tastants are detected by taste receptor cells that are clustered in taste buds. Although the majority of taste buds in humans are located on the tongue, some can also be found on the palate, pharynx, epiglottis, and upper third of the esophagus.
The gustatory system.
Tastants are detected in taste buds in the oral cavity. Taste buds on the tongue are innervated by the peripheral fibers of gustatory sensory neurons, which travel in the glossopharyngeal and chorda tympani nerves and terminate in the nucleus of the solitary tract in the brain stem. From there taste information is relayed through the thalamus to the gustatory cortex as well as to the hypothalamus.
Taste buds on the tongue occur in structures called papillae, of which there are three types based on morphology and location. Fungiform papillae, located on the anterior two-thirds of the tongue, are peg-like structures that are topped with taste buds. Both the foliate papillae, situated on the posterior edge of the tongue, and the circumvallate papillae, of which there are only a few in the posterior area of the tongue, are structures surrounded by grooves lined with taste buds (Figure 32–14A). Each fungiform papilla contains one to five taste buds, while each circumvallate or foliate papilla contains hundreds.
Taste buds are clustered in papillae on the tongue.
A. The three types of papillae—circumvallate, foliate, and fungiform—differ in morphology and location on the tongue and are differentially innervated by the chorda tympani and glossopharyngeal nerves.
B. Each taste bud contains 50 to 150 elongated taste receptor cells, as well as supporting cells and a small population of basal stem cells. The taste cell extends microvilli into the taste pore, allowing it to detect tastants dissolved in saliva. At its basal end the taste cell contacts gustatory sensory neurons that transmit stimulus signals to the brain. The scanning electron micrograph shows a taste bud in a foliate papilla in a rabbit. (Reproduced, with permission, from Royer and Kinnamon 1991.)
The taste bud is a garlic-shaped structure embedded in the epithelium. A small opening at the epithelial surface, the taste pore, is the point of contact with tastants (Figure 32–14B). Each taste bud contains approximately 100 taste receptor cells (taste cells), elongated cells that stretch from the taste pore to the basal area of the bud. The taste bud also contains other elongated cells that are thought to serve a supporting function, as well as a small number of round cells at the base, which are thought to serve as stem cells. Taste cells are short-lived and appear to be continually replaced from the stem cell population.
Each taste cell extends microvilli into the taste pore, allowing the cell to contact chemicals dissolved in saliva at the epithelial surface. At its basal end the taste cell contacts the afferent fibers of gustatory sensory neurons, whose cell bodies reside in specific sensory ganglia (Figures 32–13 and 32–14). Although taste cells are nonneural, their contacts with the gustatory sensory neurons have the morphological characteristics of chemical synapses, including clustered presynaptic vesicles. Taste cells also resemble neurons in that they are electrically excitable; they have voltage-gated Na+, K+, and Ca2+ channels and are capable of generating action potentials.
Each Taste Is Detected by a Distinct Sensory Transduction Mechanism and Distinct Population of Taste Cells
Each of the five taste qualities involves a different sensory transduction mechanism in the microvilli of taste cells. There are, however, two general types. Bitter, sweet, and umami tastants interact with G protein- coupled receptors, whereas salty and sour tastants appear to involve specific ion channels (Figure 32–15). These interactions depolarize the taste cell, leading to the generation of action potentials in the afferent gustatory fibers.
Sensory transduction in taste cells.
Different taste qualities involve different detection mechanisms in the microvilli at the apical taste pore of taste cells (see Figure 32–14B). Salty and sour tastants activate ion channels, whereas tastants perceived as bitter, sweet, or umami activate G protein-coupled receptors. Bitter tastants are detected by T2R receptors, whereas sweet tastants are detected by a combination of T1R2 and T1R3 and umami tastants by a combination of T1R1 and T1R3.
Compounds that humans perceive as sweet include sugars, artificial sweeteners such as saccharin and aspartame, a few proteins such as monellin and thaumatin, and some D-amino acids. All of these sweet-tasting compounds are detected by a complex of two related G protein-coupled receptors, T1R2 and T1R3 (Figure 32–16).
Tastants recognized by T1R and T2R receptors.
A calcium-sensitive dye was used to test whether T1R and T2R receptors expressed in a tissue culture cell line could detect tastants.
A. Cells expressing both rat T1R2 and rat T1R3 responded to a number of sweet compounds. (Reproduced, with permission, from Nelson et al. 2001.)
B. Cells expressing mouse T1R1 and mouse T1R3 responded to numerous l-amino acids (umami taste). Responses were potentiated by inosine monophosphate (IMP). (Reproduced, with permission, from Nelson et al. 2002.)
C. Cells expressing different T2R receptors responded selectively to different bitter compounds. Cells expressing mouse T2R5 responded most vigorously to cycloheximide (CYX), whereas cells expressing mouse T2R8 responded preferentially to denatonium (DEN) and 6-n-propyl-2-thiouracil (PROP). (ATR, atropine; CON, control; PTC, phenyl thiocarbamide; SOA, sucrose octaacetate; STR, strychnine.) (Reproduced, with permission, from Chandrashekar et al. 2000.)
T1R receptors have a large N-terminal extracellular domain (Figure 32–15) like the V2R receptors of vomeronasal neurons. Changing a single amino acid in this domain in mice can alter an animal's sensitivity to sweet compounds. Indeed, T1R3 was initially discovered by examining genes at the mouse saccharin preference (Sac) locus, a chromosomal region that governs sensitivity to saccharin, sucrose, and other sweet compounds.
In mice, taste cells with T1R2 receptors are found mostly in foliate and circumvallate papillae; almost invariably those cells also possess T1R3 receptors (Figure 32–17A). Gene knockout experiments in mice indicate that the T1R2/T1R3 complex mediates the detection of all sweet compounds except for high concentrations of sugars, which can also be detected by T1R3 alone.
Expression of T1R and T2R receptors on the tongue.
Sections of mouse or rat tongue were hybridized to probes that label T1R or T2R mRNAs to detect their sites of expression in taste cells.
A. T1R3 is expressed in taste cells of all three types of papillae. However, T1R1 is found mostly in fungiform papillae, whereas T1R2 is located predominantly in circumvallate (and foliate) papillae. Overlap between sites of expression appears as yellow cells in the panels at the top. The T1R1-T1R3 umami receptor is more frequently found in fungiform papillae, whereas the T1R2-T1R3 sweet receptor is more frequently found in circumvallate and foliate papillae. (Reproduced, with permission, from Nelson et al. 2001.)
B. A taste cell that detects bitter tastants can express several different T2R receptors. Here probes for T2R3 and T2R7 labeled the same taste cells in circumvallate papillae. (Reproduced, with permission, from Adler et al. 2000.)
C. T1R and T2R receptors are expressed in different taste cells. Taste cells labeled by a T1R3 probe or mixed T1R probes (green) did not overlap with cells labeled by a mixture of T2R probes (red). (Reproduced, with permission, from Nelson et al. 2001.)
Umami is the name given to the savory taste of monosodium glutamate, an amino acid widely used as a flavor enhancer. It is believed that the pleasurable sensation associated with umami taste encourages the ingestion of proteins and is thus important to nutrition.
The taste cell receptor responsible for umami taste is a complex of two related G protein-coupled receptors: T1R1 and T1R3 (Figure 32–15). In both humans and mice the T1R1/T1R3 complex can interact with all l-amino acids (Figure 32–16B), but in humans it is preferentially activated by glutamate. Purine nucleotides, such as inosine 5′-monophosphate (IMP), are often added to monosodium glutamate to enhance its pleasurable umami taste. Interestingly, in vitro studies show that IMP potentiates the responsiveness of T1R1/T1R3 to l-amino acids, suggesting that IMP acts on the receptor itself (Figure 32–16B).
Taste cells with both T1R1 and T1R3 are concentrated in fungiform papillae (Figure 32–17A). Studies in mice in which individual T1R genes have been deleted indicate that the T1R1/T1R3 complex is solely responsible for umami taste.
Bitter taste is thought to have evolved as a means of preventing ingestion of toxic molecules. Bitter taste sensations are elicited by a variety of compounds, including caffeine, nicotine, alkaloids, and denatonium, the most bitter-tasting compound known.
Bitter tastants are detected by a family of approximately 30 G protein-coupled receptors called T2Rs (see Figure 32–15). These receptors vary in protein sequence, consistent with their ability to recognize bitter compounds with diverse chemical structures. Indeed, different T2R receptors recognize different bitter compounds (Figure 32–16C). A single taste cell can express many, and probably all, types of T2R receptors (Figure 32–17B). This arrangement implies that information about different bitter tastants is integrated in individual taste cells. Because different bitter compounds are detected by the same cells, all these compounds elicit the same perceptual quality: bitter. The degree of bitterness might be caused by a compound's effectiveness in activating bitter taste cells.
Interestingly, genetic differences in the ability to perceive specific bitter compounds have been identified in both humans and mice and mapped to specific chromosomal loci. It was by examining genes at these loci that the T2R receptors for bitter tastants were first identified. In at least some cases the gene responsible for the genetic difference has proved to be a particular T2R gene. Thus, at least some bitter compounds may be recognized primarily or perhaps exclusively by only one of the 30 or so T2R receptor types.
In mice taste cells expressing T2R receptors are found in both foliate and circumvallate papillae (Figure 32–17C). Taste cells express either T2R or T1R receptors, but a single taste bud can contain taste cells of both types. Such mixing of cells accords with the observation that a single taste bud can be activated by more than one class of tastant, for example sweet as well as bitter.
Salty compounds are essential to animals for the maintenance of electrolyte balance. It is thought that their detection is mediated by specific ion channels, but the underlying mechanisms are not yet known (see Figure 32–15). Detection of sodium chloride (NaCl), for example, might result from a diffusion of Na+ ions down an electrochemical gradient through Na+ channels on taste cell microvilli, or it might involve ion channels that are opened by Na+ ions.
Sour taste is associated with acidic food or drink. As with bitter compounds, animals are innately averse to sour substances, prompting the suggestion that the adaptive advantage of sour taste is avoidance of spoiled foods.
The molecular mechanisms underlying sour stimulus transduction in the taste cell have not been identified. Detection of sour tastants may involve ion channels that are opened by H+ ions or that allow an influx of those ions that results in a depolarization of the taste cell (Figure 32–15). However, as with salty taste, the proteins responsible for sour taste transduction have not yet been defined.
Molecular-genetic studies indicate that bitter, sweet, and umami tastants are each detected by a distinct subset of taste cells. As already discussed, a combination of T1R1 and T1R3 is responsible for all umami taste, while a combination of T1R2 and T1R3 is needed for all sweet taste detection except for the detection of high concentrations of sugars, which can be mediated by T1R3 alone. T1R1 and T1R2 are expressed by separate subsets of taste cells, indicating that the detection of sweet and umami tastants is segregated.
In mice a transduction protein (PLCb2) is required for detection of bitter, sweet, and umami tastants. When this protein is expressed only in cells with bitter receptors, the cells are responsive to bitter compounds but not to sweet compounds or amino acids. This result confirms that taste cells that detect bitter compounds are distinct from those that detect sweet and umami tastants. Taste cells that detect salty and sour tastants may form two additional subsets of cells.
Studies in mice further indicate that it is the taste cells rather than the receptors that determine the animal's response to a tastant. The human bitter receptor T2R16 recognizes a bitter tastant that mice cannot detect. When this receptor was expressed in mouse taste cells that express the T1R2/T1R3 sweet complex, the human T2R ligand elicited an attractive response; when it was expressed in mouse cells that express T2R bitter receptors, the same ligand instead caused aversion. These findings suggest that innate responses of mice to sweet and bitter compounds result from specific gustatory pathways (labeled lines) that link the activation of different subsets of taste cells to different behavioral outcomes.
Sensory Neurons Carry Taste Information from the Taste Buds to the Brain
Each taste cell is innervated at its base by the peripheral branches of the axons of primary sensory neurons (Figure 32–14). Each sensory fiber branches many times, innervating several taste cells within numerous taste buds. The release of neurotransmitter from taste cells onto the sensory fibers induces action potentials in the fibers and the transmission of signals to the sensory cell body.
The cell bodies of gustatory sensory neurons lie in the geniculate, petrosal, and nodose ganglia. The peripheral branches of gustatory sensory neurons in these three ganglia travel in cranial nerves VII, IX, and X (Figure 32–13).
The central branches of axons of the gustatory sensory neurons enter the medulla, where they terminate on neurons in the gustatory area of the nucleus of the solitary tract (Figure 32–13). In most mammals neurons in this nucleus transmit signals to the parabrachial nucleus of the pons, which in turn sends gustatory information to the ventroposterior medial nucleus of the thalamus. In primates, however, these neurons transmit gustatory information directly to the taste area of the thalamus.
Taste Information Is Transmitted from the Thalamus to the Gustatory Cortex
From the thalamus taste information is transmitted to the gustatory cortex, a region of the cerebral cortex located along the border between the anterior insula and the frontal operculum (Figure 32–13). The gustatory cortex is believed to mediate the conscious perception and discrimination of taste stimuli. The taste area of the thalamus also transmits information both directly and indirectly to the hypothalamus, a structure that controls feeding behavior and autonomic responses.
Recordings made from neurons in the gustatory cortex indicate that some neurons respond to different classes of tastants, whereas others respond to only one, such as bitter or sweet. It might be that neurons responsive to more than one class of tastants encode information about blends whereas those in gustatory cortex or other areas that respond to single taste categories are involved in innate responses, such as attraction to sweet tastants or aversion to bitter tastants.
Perception of Flavor Depends on Gustatory, Olfactory, and Somatosensory Inputs
Much of what we think of as the flavor of foods derives from information provided by the olfactory system. Volatile molecules released from foods or beverages in the mouth are pumped into the back of the nasal cavity by the tongue, cheek, and throat movements that accompany chewing and swallowing. Although the olfactory epithelium of the nose clearly makes a major contribution to sensations of flavor, such sensations are localized in the mouth rather than in the nose.
The somatosensory system is thought to be involved in this localization of flavors. The coincidence between somatosensory stimulation of the tongue and the retronasal passage of odorants into the nose is assumed to cause odorants to be perceived as flavors in the mouth. Sensations of flavor also frequently have a somatosensory component that includes the texture of food as well as sensations evoked by spicy and minty foods and by carbonation.
Insect Taste Organs Are Distributed Widely on the Body
Like vertebrates, insects have specialized organs for taste. Some of the taste neurons occur in internal mouth parts. Others lie near the mouth on the proboscis, or are scattered on the leg, wing, and oviposition organs.
The gustatory receptors of Drosophila are membrane- spanning receptors that are very distantly related to the odorant receptors of the fly. The fly has approximately 60 gustatory receptor genes, a surprisingly large number considering it has approximately 60 olfactory receptor genes. Members of the gustatory receptor gene family are expressed in all of the different kinds of taste organs. Some occur in particular cell types, whereas others are present in many parts of the body.
As in vertebrates, in flies numerous taste receptor genes appear to be expressed in a single neuron. Sweet-sensing and bitter-sensing neurons in the labial palp mediate food acceptance or rejection, respectively. Other neurons have distinct functions. For example, neurons in the male leg express gustatory receptors that are involved in recognizing females during courtship.