Common sense about taste: from mammals to insects

Abstract

The sense of taste is a specialized chemosensory system dedicated to the evaluation of food and drink. Despite the fact that vertebrates and insects have independently evolved distinct anatomic and molecular pathways for taste sensation, there are clear parallels in the organization and coding logic between the two systems. There is now persuasive evidence that tastant quality is mediated by labeled lines, whereby distinct and strictly segregated populations of taste receptor cells encode each of the taste qualities.

Figure 1. The Anatomy of Taste

Taste buds are broadly distributed on the tongue and soft palate. On the tongue, taste buds are localized to three classes of papillae: In mice, the single circumvallate papilla is found at the very back of the tongue; foliate papillae are at the posterior lateral edge, and fungiform papillae are distributed over the anterior two thirds of the tongue; these three classes of paplilae can be highlighted in mice engineered to express green fluorescent protein in taste bud areas (lower right panel). The taste buds on the tongue and palate are innervated by three afferent nerves: the chorda tympani, greater superficial petrosal, and glossopharyngeal. These nerves carry taste information from the taste receptor cells to the nucleus of the solitary tract (NST) in the brain stem. From the NST, taste responses are transmitted (and processed) through the parabrachial nucleus (PbN) and the thalamus (VPM) to the primary gustatory cortex in the insula. Behavioral responses to food (and perceptions of flavor) are ultimately choreographed by the integration of gustatory information with other sensory modalities (such as olfaction, texture, etc.)

Figure 2. Mammalian Taste Receptors, Cells, and Ligands

Detection of the gustatory world is mediated by several distinct classes of taste receptors and taste receptor cells. Sweet and umami compounds are sensed by T1R heterodimers (Nelson et al., 2001, 2002; Li et al., 2002), while bitter compounds activate T2R receptors (Chandrashekar et al., 2000; Mueller et al., 2005; Meyerhof et al., 2005). Salt is detected via several mechanisms, one of which is thought to rely on the sodium channel ENaC (Heck et al., 1984). Sour-sensing cells are defined by the expression of PKD2L1 (Huang et al., 2006), whereas gustatory responses to carbonation are mediated by the membrane-tethered carbonic anhydrase CA IV (Chandrashekar et al., 2009).

Figure 3. Labeled Lines Mediate Taste Sensation

It is now known that tastes to sweet (red), bitter (blue), sour (green), umami (yellow), and sodium (purple) are mediated by separate populations of selectively tuned taste receptor cells. Notably, taste buds from all regions of the oral cavity contain cells that respond to the five basic modalities. Thus, contrary to popular belief, there is no topographic map (i.e., a tongue map) of taste qualities on the tongue.

Figure 4. Behavioral Attraction and Aversion Are Hardwired

Mice and flies have converged on a similar organization of taste coding at the periphery. In both cases, dedicated cells tuned to selective taste qualities are hardwired to trigger specific behavioral responses. The synthetic opiate spiradoline is normally tasteless to mice (A, open circles). However, after targeted expression of the spiradoline receptor (RASSL) to sweet cells, mice exhibit dose-dependent attraction to spiradoline (Zhao et al., 2003). In marked contrast, directing expression of the very same RASSL receptor to bitter cells results in strong aversion to the ligand (Mueller et al., 2005). Similarly, activation of selective populations of gustatory receptor neurons in flies (B) mediates robust innate behavioral responses (Marella et al., 2006). Expression of the mammalian ion channel TrpV1 in sugar-sensing GRNs (Gr5a-TrpV1) results in strong behavioral preference for capsaicin. In contrast, expression of TrpV1 in the “bitter-responsive” Gr66a cells makes capsaicin an aversive tastant. Normal flies do not respond to capsaicin (open circles); preference index = (tastant − control)/total.

Figure 5. Fly Taste Reception

(A) Flies detect tastants via gustatory receptor neurons (GRNs) housed in sensilla distributed across the mouth parts (labella), legs, and wings. Stimulation of GRNs by appetitive tastants elicits extension of the proboscis to initiate feeding. Upon intake, food contacts GRNs in the taste pegs of the inner labellum and in the internal taste organs lining the pharynx (lateral sensory organ, ventral cibarial organ, and dorsal cibarial sensory organ). (B) Like mammals, fly gustatory receptors are expressed into dedicated classes of GRN detecting distinct classes of attractive or aversive tastants. Most, but not all, sugar and bitter receptors are members of the “Gustatory Receptor” (Gr) gene family (Montell, 2009; Al-Anzi et al., 2006; Mitri et al., 2009). To date, several Grs have been linked to detection of specific attractive or aversive tastants. For example, mutants for Gr66a and Gr93a both show defective behavioral and physiological responses to caffeine (Lee et al., 2009); logically, as fruit flies are not normally exposed to caffeine, this receptor must be activated by ligands sharing structural features with caffeine. As for sugar detection, Gr64f is a candidate receptor required for responses to a wide range of sugars, including sucrose, maltose, glucose, and trehalose (Dahanukar et al., 2007; Jiao et al., 2008; Slone et al., 2007). In contrast, Gr5a is a narrowly tuned receptor for trehalose alone (Chyb et al., 2003). Thus, many receptors may recognize the same sugars, and a given sugar may act on several receptors (or receptor complexes). Carbonation and water are sensed by different subpopulations of GRNs (Fischler et al., 2007; Inoshita and Tanimura, 2006).