Functional Anatomy of the Gustatory System: From the Taste Papilla to the Gustatory Cortex
General Aspects of Taste Sensation
Taste sensation is one of the five sensory modalities, activated by chemical stimuli that react with taste organs on the oral epithelium.
Five basic or fundamental tastes (i.e., taste quality) are described; sweet, salty, sour, bitter, and umami. Sweetness is caused by sucrose or artificial sweeteners such as saccharin; saltiness solely by sodium chloride and lithium chloride; sourness by inorganic and organic acids; bitterness by various substances, such as urea or quinine; and umami by monosodium glutamate and nucleoside monophosphates. Sweet and umami represent energy sources or innate rewards; salty, the balance of minerals; acid, the signal of putridity; and bitter, that of toxins (with some exceptions, such as white lead tasting sweet).
Some specific areas of the tongue or palate have been thought to be most responsive to one particular taste, but this has been proven incorrect and there is large individual variation in the regional specificity of taste responsiveness.1
A mixture of two or more tastants sometimes causes increased or decreased taste sensations compared with the sum of taste intensities caused by each of the component tastants alone (mixture facilitation or suppression, respectively).2 In most cases, this occurs at the peripheral level (e.g., receptor sites). Mixture facilitation is seen in synergistic responses between two different umami substances.3
Localization of taste stimuli is poor compared with that of tactile stimulation,1 and is achieved with the aid of tactile sensation. When chemicals are applied to both sides of the tongue, the intensity of the tastant or the location of the sensation changes,4 and central mechanisms are probably involved in this.
All aspects of taste sensation are not fully studied in humans. This chapter reviews taste reception in rodents, and neural pathways and coding in monkeys, on which our knowledge of the human gustatory system is largely based. Finally, recent findings from noninvasive studies of human gustatory cortices are reviewed.
Taste Reception
Taste Buds: Taste Receptor Organs
Taste buds (gemmae) are taste receptor organs located on the tongue, palate, and pharynx ( Fig. 13.1 ).5 They are 70 µm in length, and 40 µm in width. Electron microscopy reveals that a taste bud contains 30 to 80 elongated cells together with a few basal cells inside the capsule. Three different types of elongated cells are identified: dark cells or supporting cells (type I; constituting 55 to 75% of taste bud cells), light cells (type II; 15 to 30%), and intermediate cells (type III; 5 to 15%). One or two basal cells (type IV) are also recognized ( Fig. 13.1 ).6 Types I, II and III cells bear microvilli that project from the apical dendrites toward the taste pore (the opening to the oral cavity), and are connected by tight junctions at the apical dendrites so that tastants and salivary fluid cannot access the lateral or basal surface of the cell membrane within the taste bud. The taste pore is filled with mucus, but the tip of the microvilli of some cells projects above this to receive tastants. Type I cells contain secretory granules containing mucous substances. Type III cells possess microfilaments similar to neurons, making synaptic contacts with nerve terminals and various synaptic vesicles at the presynaptic area.6 Type II cells do not.
Type IV cells, situated at the base of the taste bud, are round with a lobulated nucleus. Some type IV cells express the Sonic hedgehog protein, and may be a transient precursor of types I to III cells and a signal center for the proliferation of progenitor cells in the taste buds.7 At the basal pore, a few small nerve fibers (intragemminal fibers) enter the taste bud.
The lifespan of the taste bud cells is very short at around 10.5 days,8 although a much longer lifespan is noted for some taste receptor cells.9
Taste Papillae
There are four kinds of papilla on the tongue. Three of them bear taste buds and are called the taste papillae ( Fig. 13.1 ), although taste buds also exist independently in the epidermis of the soft palate or pharynx. Among taste papillae, fungi-form papillae (0.7 to 2 mm in diameter) are found on the anterior two-thirds of the tongue and bear an average of 3.5 taste buds on top,10 although some fungiform papillae (12.8 to 63%) lack taste buds completely.10 Foliate papillae, consisting of as many as 20 ridges and furrows, are situated on each side of the posterior tongue.10 Circumvallate papillae, concentrically grooved structures with a diameter of 4 to 8 mm, are located in front of the terminal sulcus. Most people have between 4 and 18 (average of 9.2 ± 1.8) circumvallate papillae.10 Both foliate and circumvallate papillae bear a large number of taste buds deep in the trench where the taste pores open. Filiform papillae bear no taste buds and are characterized by a cornified layer on the top of the epithelium.
The total number of taste buds on the tongue is up to 4,600 in humans: 24% on fungiform papillae, 28% on foliate papillae, and 48% on circumvallate papillae.11 More taste buds are located on the posterior tongue than on the anterior tongue.
The density of fungiform papillae on the anterior tongue can be examined. It is high at the tongue tip (24.5 /cm2; range 2.4 to 80), but low on the median dorsum (8.2 /cm2; range 0 to 28.3).11 The number of taste buds varies individually, and, in contrast to previous reports, does not decline with age.11 Patients who can taste phenylthiocarbamide (PTC) or 6-n-propylthiouracil (PROP) have a larger number of taste buds than those who cannot.11 The threshold of detection of a certain tastant is lower when a tongue area with a higher density of taste buds is stimulated.12
Although it is reported that single fungiform papillae are sensitive to a single basic stimulus,4 they are often sensitive to a few tastants. About 65% of papillae examined have been found to be sensitive to at least three of four tastants tested, 20% sensitive to a single tastant, and 13% not sensitive at all.13
Innervation of Taste Papillae and Taste Buds
Several nerve fibers enter a single fungiform papilla, some of which send collaterals to neighboring papillae. This means that a single taste fiber can innervate several taste papillae.12 On average, a single fiber innervates one to four papillae.11
Fungiform papillae are innervated by the chorda tympani (CTN), a sensory branch of the facial nerve; foliate papillae by both the CTN and a lingual branch of the glossopharyngeal nerve (GLN); and circumvallate papillae by the GLN ( Fig. 13.1 ). Taste buds in the soft palate are innervated by the superficial greater petrosal nerve (SGP), another sensory branch of the facial nerve, while those in the pharynx are innervated by the supralaryngeal nerve, a sensory branch of vagal nerve (VN).
Taste Receptors and Taste Transduction
Type II cells in the taste bud express G-protein coupled receptor proteins for sweet, umami, or bitter, while type III cells express ionic taste receptors for salty or sour tastants. Taste signals may be integrated within the taste buds before being transmitted to the taste nerves.
The taste receptors for sweet, bitter, and umami are G protein–coupled receptor proteins (GCRPs). They are seven transmembrane domain receptor proteins with an N-terminal in the extracellular space and a C-terminal associated with G protein in the intracellular space. Taste receptors are believed to be located at the apical microvilli of taste receptor cells (TRCs). They can be classed as type 1 (T1R) or type 2 (T2R). T1Rs are class C GCRPs with a long N-terminal, whereas T2Rs are class A GCRPs with a short N-terminal.15 T1R1, T1R2, and T1R3 are themselves orphan receptor proteins, but a heterodimer of T1R2 + T1R3 is sweet receptor, and that of T1R1 + T1R3 is umami receptor ( Fig. 13.2 ).15 Twenty-five T2Rs are involved in receiving bitter tastants in humans, and different T2Rs are concerned with different bitter tastants15 (e.g., T2R4 for denatonium, T2R38 or T2R44 for PTC or PROP, and T2R43 or T2R44 for saccharin). A taste version of metabotropic glutamate receptor type 1 or 4 (taste mGluR1 and mGluR4) is also presumed to be the receptor protein for glutamate, but, unlike T1R1 + T1R3, does not yield synergistic responses to a mixture of glutamate and ribonucleotide.16 In the mouse, T1Rs and T2Rs are expressed in different TRCs, but almost all T2Rs are expressed in the same TRC.15
Salty or sour taste receptors have not been fully elucidated. The degenerin/epithelial sodium channel (EnaC) family has been suggested,16 with the selective amiloride-sensitive ENaC proposed as a candidate for the salty taste receptor16 (with no convincing evidence), and a neuronal (degenerin) amiloride-sensitive cation channel, including an acid-sensing ion channel (ASCIC), proposed as a candidate receptor for sour taste.17,18 A heterodimer of polycystic kidney disease protein 1L3 and 2L1 (PKD2L1) has also been proposed as the sour receptor,15,16 and its involvement in human sour taste has been reported.14,15
GCRPs are expressed in type II cells, whereas ionic channel receptors for acid or salt are located in type III cells.14,15 Therefore, type II cells are now called receptor cells and type III cells are presynaptic cells.
Taste Transduction
Sodium or lithium ions enter ENaCs to depolarize taste cells, an action that is partly inhibited by amiloride. Protons (H+) activate ASCIC or PKD2L1 to open an ionic channel and depolarize cells.
Sweet, bitter, or umami substances react with GCRPs, leading to activation of a G protein (gustducin in T2Rs15), which triggers an intracellular cascade common to TRCs expressing either T1R or T2R: activation of phospholipase Cβ2; production of inositol-1,4,5-triphosphate; calcium ion release from intracellular calcium stores; and finally stimulation of transient receptor potential (TRP) protein TRPM5 to depolarize cells ( Fig. 13.3 ).15,16 Transduction of sweet tastant is blocked by gymnemic acids.
Type II cells release adenosine triphosphate from pannexin 1 hemichannels, into the intracellular space, which activates type III cells with purinergic receptors and probably taste nerve fibers by paracrine secretion ( Fig. 13.3 ).17 Type III cells activate taste fiber terminals via synapses. Thus, type III cells as well as taste fibers are able to respond to organic tastants.17 Chemicals such as serotonin or glutamate have been suggested as synaptic transmitters between type III cells and nerve terminals.18,19
Temperature dependence of taste transduction has been noted in taste psychophysics20 and the physiology of taste fibers.21 Most taste responses have an optimal temperature of 30°C, except sodium chloride, which has an optimal temperature of 10°C or lower, suggesting the presence of an energy barrier for chemical reactions between tastants and receptors. However, it is partially ascribed to the temperature dependence of TRPM5.22
Responsiveness of Taste Receptor Cells
Electrophysiology has shown that TRCs generate depolarizing receptor potentials in response to tastants,23 but can also produce sodium spikes because of the presence of sodium channels.24 In mice, type II cells differentially respond to umami, sweet, or bitter, while type III cells respond to salt or sour tastants.16
Peripheral Taste Nerves
Course of Taste Nerves
The CTN and SGP take a peripheral course toward the taste buds, together with the lingual branch (LN) or palatal branch of the trigeminal nerve. They take a complex central course to the medulla to terminate in the solitary tract nucleus (NTS) ( Fig. 13.4 ).
The CTN travels to the tympanic cavity, where it runs near the auditory ossicles. It then enters the facial canal to form the geniculate ganglion, and to fuse with the SGP to form the intermediate nerve of Wrisberg (IMN), which joins the facial nerve. After leaving the soft palate, the SGP traverses the sphenopalatine ganglion to the tympanic cavity, with its cell body in the geniculate ganglion. The IMN enters the cranium, diverges from the facial nerve, and enters the solitary tract in the medulla. A somatosensory branch innervating the pinna joins the facial nerve in the canal. The GLN runs just underneath the pharyngeal epithelium to innervate foliate or circumvallate papillae. The GLN forms the petrosal ganglion, and the VN forms the nodosal ganglion. The latter two enter the cranium to the solitary tract. In humans, all three taste nerves enter the solitary tract before terminating in the NTS, while in monkeys the IMN and GLN do not.25
The IMN, GLN, and supralaryngeal nerves contain large and small somatosensory fibers. The IMN and GLN also contain autonomic nerve fibers innervating salivary glands. The conduction velocity of taste fibers is similar to that of myelinated or unmyelinated fibers.26
Response Profile of Taste Nerve Fibers: Neural Taste Information
Single taste fibers are responsive to a single or a few basic tastants depending on the species of animal. In monkeys and mice, single taste fibers generally respond to a single basic taste, but in rats and cats they respond to multiple basic tastes. The responsiveness of taste fibers to various tastants is often expressed in terms of the tastant that produces the largest response of the four or five basic tastes (best-stimulus category).27 When tastants are arranged in the order of sweet, salt, sour, and bitter along the abscissa, and response magnitudes are plotted on the ordinate, the response profile of single taste fibers has a single peak in each best-stimulus category in the CTN and GLN.27
In monkeys, single CTN fibers are most responsive to sweet, salty, or sour substances, but rarely to bitter or umami substances, whereas single GLN fibers best respond to sweet, bitter, and umami substances ( Fig. 13.5 ).28–30 In rats, umami mixtures evoke synergistic effects in the CTN (the sweetresponsive fibers in particular31) but not in the GLN. In rodents, the whole SGP bundle is more responsive to sweet substances than the CTN.32 However, single-fiber analysis does not confirm this finding. Most single fibers in the supralaryngeal nerve are responsive to water in rabbits or rats, and this response is inhibited by addition of ions.33 The CTN of primates also yields responses to water.34
Each of the taste nerves innervates different regions of the oral cavity, conveying various characteristics of taste signals. They take their own courses to the central nervous system where they may be damaged during surgical procedures, e.g., surgery of the middle ear.
Central Pathways: Taste Relay Nucleus and Related Structures
Nucleus of the Solitary Tract
Anatomy
The NTS is located at the dorsal medulla. The anterior portion lies ventral to the dorsal vestibular nucleus and the posterior portion fuses with the contralateral counterpart to make the nucleus communicans near the obex, the posterior end of the rhomboid fossa. In monkeys, the NTS is histologically subdivided into the lateral and medial subnucleus.25 The anterior portion, made of the lateral subnucleus, is the first relay of the central gustatory pathway. The IMN enters the NTS posterior to the entry of the facial nerve, followed by the GLN, and the VN most posteriorly.25 The IMN and GLN terminate at the lateral subnucleus, while the VN terminates at both subnuclei.25 The lateral subnucleus probably contains taste neurons. The human NTS is subdivided into ten subnuclei, among which the interstitial subnucleus corresponds to the lateral subnucleus in monkey.25 Somatosensory components of taste nerves, including the facial nerve innervating the pinna, terminate at the nucleus of the spinal tract of the trigeminus.
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