6.1. INTRODUCTION

Taste stimuli are unique in the world of recognizable objects, in that they are perceived only after being selected and engulfed (Figure 6.1). The physical sources of your current visual, auditory, somatosensory, and olfactory percepts are essentially external—you see what’s in front of your face, hear what’s within earshot, feel what’s within reach, and smell bits of external objects carried to you in the airstream (it is usually possible to determine from whence it was dealt once it has been smelt)—but a stimulus activates the gustatory system only after it has been purposefully removed from view. Organisms make a deliberate decision to have a taste experience, choosing an external object in their environment for consumption and experiencing the taste percept only after sending that object down the path toward digestion.

FIGURE 6.1

Egocentric distances of the five senses (units in Biblical proportions). At the top are two paintings showing Eve in the Garden of Eden. At the left is a detail from H. Bosch’s Last Judgment and at the right is a detail from W. Blake’s (more...)

This concrete, physical difference between taste and other stimuli has important bio-psychological implications: stimuli providing taste sensations affect well-being with a reliability that other stimuli do not. The five major categories of taste quality are all tuned to identify a specific nutrient or physiological threat, namely ensuring energy reserves (sweet), maintaining water balance (salty), guarding pH (sour), motivating protein intake (savory), and avoiding toxins (bitter, see Bartoshuk 1991). A smell can be noxious, a sound too loud, a touch too rough, or an image too dangerous/titillating for safe viewing, but the vast majority of such stimuli leave little physiological trace once they’ve passed by. Because tasty stimuli are already in the body when perceived (at least for mammals), however, they directly impact our health and happiness. They feed and fatten us, poison, pickle, or please us, replenish or repulse us, but they seldom leave us unaffected.

It is perhaps the fact that tastes invariably impact what Garcia referred to as the internal milieu (Garcia, Hankins, and Rusiniak 1974) that makes them by far the most directly rewarding (or punishing) of the sensory stimuli. Taste stimuli act as primary reinforcers in a wide variety of contexts (Berridge 1996; O’Doherty et al. 2002; Hajnal and Norgren 2005); in fact, most other stimuli reinforce on the basis of temporal association with basic tastes (Gallagher and Schoenbaum 1999; Balleine and Dickinson 2000; O’Doherty et al. 2003). Although it is true that both human and non-human primate males will pay to access naked images of female conspecifics (Deaner, Khera, and Platt 2005), visual, auditory, somatosensory, and olfactory stimuli are seldom as tightly linked to reward as are stimuli imbued with taste attributes. Put succinctly, most sensory stimuli are used to attain reward, but thanks to their privileged access to the internal milieu, tastes are rewards. ^*

In the essay that follows, we will discuss what is known about taste in this context. We will first provide a brief anatomical overview of the gustatory system, and then describe taste-related behaviors and their underlying neurobiology, with particular consideration of the intimate links between taste and reward (for a comprehensive discussion of the link between post-ingestive effects and reward, see Chapter 12). We will go on to describe incentive learning research, which, while seldom discussed in these terms, demonstrates the ease with which intrinsic reward values of tastes can be transferred to temporally associated stimuli. We will suggest that this ease reflects an evolutionary imperative: the animal that survives will most likely be the one that is easily and strongly motivated by the sight, sound, and smell of an external object associated with this taste reward; thus, animals come equipped with strong connections between taste and the other sensory systems. This line of thinking—all of which follows more or less directly from the basic physical fact that taste sensations are unique in emanating from inside the body—leads us to a new conception of “flavor” as a byproduct of an evolutionary necessity, that of connecting all stimuli with the rewarding properties of taste.

6.2. THE TASTE SYSTEM ITSELF

Tastes activate receptor cells in taste buds. The taste receptor cells appear to respond quite specifically to particular taste types (Yarmolinsky, Zuker, and Ryba 2009), although some evidence suggests that the “output” cells in the taste buds (a subset entirely distinct from those carrying transductive machinery, see Roper and Chaudhari 2009) may integrate information from multiple types of receptor cells (Tomchik et al. 2007). Cranial nerves VII, IX, and X carry this information to the nucleus of the solitary tract (NTS), which in turn projects (in rodents) to the parabrachial nuclei (PbN) of the pons, and to medullary motor nuclei (Norgren 1978). Neurons in both regions respond to the quality and concentration of tastes (Di Lorenzo 1988; Nishijo and Norgren 1990; Nakamura and Norgren 1991; Di Lorenzo and Victor 2003); these responses, which vary from narrowly to broadly tuned, ^* are sufficient to drive taste-specific ingestive and defensive behaviors in the absence of a forebrain (Grill and Norgren 1978b), but the behavioral repertoire may be abnormal (Grill and Norgren 1978b; Flynn and Grill 1988).

Beyond this brainstem circuit, the taste system becomes quite complex. Axons carry taste information from the pons (again, in the rodent) to the forebrain along three separate paths: one to the insular gustatory cortex (GC) via the parvicellular division of the ventroposteromedial (VPM) nucleus of the thalamus (Kosar, Grill, and Norgren 1986), one to the amygdala (Ottersen 1981), and one to the hypothalamus (Norgren 1974). While the cortical and limbic projections have been suggested to have distinct functions (Norgren, Hajnal, and Mungarndee 2006), they are closely related in a number of ways. In each, for instance, taste inputs are integrated with those from other sensory systems: GC receives somatosensory inputs from the oral cavity (Barnett et al. 1995) and olfactory inputs from the endopiriform nucleus (Fu et al. 2004), and amygdala receives auditory and visual cortical inputs (McDonald 1988). The hypothalamus receives interoceptive input from areas without a blood-brain barrier (Camargo, Saad, and Camargo 2000) and has a direct influence on sympathetic and parasympathetic outputs (van den Pol 1999). Of note, and as discussed later in this essay, the relay between NTS and PbN has not been identified in the primate gustatory system (Beckstead, Morse, and Norgren 1980; Norgren 1990; Pritchard, Hamilton, and Norgren 2000); instead, NTS projects directly to the VPM thalamus.

Cross-talk renders the relationships among the three parallel taste pathways explicit: the basolateral nucleus of the amygdala (BLA) is reciprocally connected with GC (McDonald and Jackson 1987; Shi and Cassell 1998), and the central nucleus of the amygdala (CeA) receives information from both GC (Turner and Zimmer 1984; McDonald 1988) and BLA (Savander et al. 1995); the lateral hypothalamus is reciprocally connected with CeA (Ottersen 1981) and GC (Allen et al. 1991). Finally, each of these structures feed back to the pons and medulla, ensuring that all but the first few milliseconds of taste responses are informed by processing in each pathway (Di Lorenzo 1990; Lundy and Norgren 2001, 2004).

6.3. TASTE-RELATED BEHAVIORS ARE INEVITABLE EXPRESSIONS OF INHERENT REWARD VALUE

Researchers routinely perform experiments in which conscious animals watch, feel, or listen to stimuli without making discernible behavioral responses. Although part of the explanation for this fact lies in the frequent use of stimuli lacking ethological validity (Weliky et al. 2003; Felsen and Dan 2005), even stimuli that provoke a specific response in an animal’s natural environment (e.g., species-specific calls) often fail to do so in laboratory contexts (Ghazanfar and Santos 2004).

Activation of the above-described taste system, in comparison, can seldom be observed passively: to wit, ingestion requires the active hand-to-mouth (paw-to-maw) participation of the subject. The most basic taste-related behaviors—orofacial responses referred to as “taste reactivity” (Grill and Norgren 1978a)—are reflex-like in their inevitability and reliability. Put a sample of something bitter into the mouth of a rodent, primate (Rosenstein and Oster 1988), or even amphibian (Liversedge 2003), and it will produce yawning “gapes” indicative of aversion. A drop of sweet fluid, meanwhile, induces lateral licks that indicate pleasure, and a mildly acidic taste causes a mixture of the two responses. These responses are evaluative in that they reveal a taste’s hedonic properties (i.e., how much that particular animal “likes” the taste; Berridge 2000) and have even been used to suggest that taste palatability comprises a relatively simple continuum (Breslin, Spector, and Grill 1992).

Gapes and licks reflect the animal’s desire to have less of or gain more of the substance affiliated with the taste, respectively. They inform an observant experimenter of the animal’s taste preferences. Similarly, various measurements of an animal’s consumption (Flynn, Culver, and Newton 2003; Caras et al. 2008), including the number and speed of licks at briefly available lick spouts (Davis 1973; Boughter et al. 2002; Zhang et al. 2003), and relative consumption of two simultaneously or sequentially available bottles (Touzani, Taghzouti, and Velley 1997; Curtis et al. 2004; Danilova and Hellekant 2004), reveal ubiquitous preference behavior generated by taste delivery.

While any one of these tasks can in some circumstances be dissociated from the others (Berridge 1996; Caras et al. 2008), what is reliable is that tastes have an intrinsic value that is far less obvious for stimuli in other modalities. As just one example, preferential looking tasks are frequently described in the literature, but with the exception of a few powerful visual stimuli (Deaner, Khera, and Platt 2005), preferences in infants typically reflect familiarity rather than inherent value judgment (for two of many examples, see Weizmann, Cohen, and Pratt 1971; Slater 2004); in taste, familiarity is just one variable that modulates the inevitable preference judgment, and its influence on preference is complex (De la Casa, Diaz, and Lubow 2003; Reilly and Bornovalova 2005; Rubin et al. 2009). Taste values can change with increasing familiarity, with taste (Garcia et al. 1985) and non-taste experience (Galef et al. 1997; Plassmann et al. 2008; Fortis-Santiago et al. 2010), and with physiological needs (Prakash and Norgren 1991), but value itself is an unavoidable part of taste perception.

6.4. THE INTERCONNECTEDNESS OF TASTE- AND REWARD-PROCESSING SYSTEMS IN THE BRAIN

Given that value is an intrinsic part of taste behaviors, it is unsurprising that value also turns out to be an intrinsic part of activity in the neural taste system. The ubiquity of value judgments in taste perception is reflected in the strong palatability-related information contained in neural taste responses from these regions. In awake rodents, palatability information has been observed in five- to ten-second averages of single neuron spike trains in the central amygdala (Nishijo et al. 1998), one of the primary targets of brainstem taste relays (Norgren 1976). Similar results have been reported for the pontine and medullary sources of these projections themselves (Scott and Mark 1987; Nishijo and Norgren 1997). Recent intrinsic signal imaging data, meanwhile, suggest that the spatial distribution of taste responses in primary GC is also palatability-related (Accolla et al. 2007), and while scant information is specifically available on taste responses in rodent orbitofrontal cortex (OFC, see de Araujo et al. 2006; Gutierrez et al. 2006), the large literature on incentive learning suggests that OFC codes tastes in a value-related manner (Gallagher, McMahan, and Schoenbaum 1999). Recent studies further suggest that GC and amygdala contain epochs within the time courses of their responses in which palatability-related information dwells (Katz, Simon, and Nicolelis 2001; Fontanini and Katz 2006; Fontanini et al. 2009). Clearly, value is a central facet of taste responses across the gustatory neuroaxis of rodents.

In primates, which again seem to possess neither a pontine taste relay (Pritchard, Hamilton, and Norgren 2000; Topolovec et al. 2004) nor direct brainstem-to-amygdala connections (Beckstead, Morse, and Norgren 1980), the picture is less clear. OFC may play a privileged role in encoding value in primates. Imaging studies suggest that OFC responds differentially to palatable and aversive tastes, and that the valence-specific taste responses are independent of intensity (Small et al. 2003) and quality (Small et al. 2001; Kringelbach et al. 2003; Small et al. 2008). In addition, when subjects are asked to evaluate the pleasantness of a taste, the OFC is selectively engaged (Small et al. 2007; Grabenhorst and Rolls 2008).

Still, there is substantial evidence that primate GC and amygdala also respond in a palatability-specific manner to taste input. In GC, early reports suggested that satiety-induced changes in taste pleasantness did not affect GC responses (Rolls, Sienkiewicz, and Yaxley 1989), but fMRI data in humans suggests that many manipulations of palatability do in fact modulate GC responsiveness (Berns et al. 2001; Small et al. 2001; Nitschke et al. 2006; Smeets et al. 2006). The data from amygdala are more mixed, with electrophysiology from non-human primates (Yan and Scott 1996) converging with some human imaging studies (Zald et al. 1998) to suggest that amygdalar neurons respond differentially to palatable and aversive tastes (for analogous data regarding visual stimuli, see Paton et al. 2006), while other fMRI data suggest that the amygdala is more responsive to taste intensity than taste hedonics (Small et al. 2003). This latter result may reflect genuine interspecies differences; on the other hand, if neurons responding to either pleasant or unpleasant taste are highly intermingled in amygdala (as the rodent electrophysiology suggests, see Fontanini et al. 2009), then these differences might be beneath the spatial resolution of the fMRI technique.

The fact that taste-driven neural activity and behaviors are intrinsically value-laden suggests that tastes must also activate brain regions directly involved in the coding of stimulus value, and that these regions must feed back into the main taste neuroaxis. The obvious candidate is of course the dopamine system, widely agreed to be centrally involved in tagging experiences and stimuli as rewards (Schultz et al. 1995; Schultz 2001). In fact, recent research confirms the suspicion that taste stimuli activate neurons within the rodent nucleus accumbens (Roitman, Wheeler, and Carelli 2005) and ventral pallidum (Tindell et al. 2006), regions known to be involved in dopamine-linked reward processes (Berridge 1996; Cardinal et al. 2002; Kelley et al. 2002; Pecina and Berridge 2005). Furthermore, direct measurements show that palatable tastes are potent stimulators of dopamine release (Ahn and Phillips 1999; Hajnal and Norgren 2001), and that both systemic administration of dopamine antagonists and dopamine depletion of the ventral tegmental area (VTA, the primary source of accumbens dopamine, see Oades and Halliday 1987) inhibit consumption of such tastes (Roitman et al. 1997; Martinez-Hernandez, Lanuza, and Martinez-Garcia 2006). Taste-induced dopamine activity is increased even by sham feeding (Frankmann et al. 1994; Liang, Hajnal, and Norgren 2006), a fact that squarely implicates orosensory stimulation as the activity’s cause.

These data indicate that the dopamine system is intimately intertwined with the taste system. A combination of anatomical and behavioral/lesion data reveal the nature of this relationship. In mouse, the pontine taste relay is directly and reciprocally connected to the VTA (Tokita, Inoue, and Boughter 2009). Taste-related dopamine activity in accumbens (and elsewhere) is not driven by this direct connection, however. Studies indicate that it is the amygdalar feedback pathway that is vital for taste-induced accumbal dopamine release (Ahn and Phillips 2002; Hajnal and Norgren 2005). Thus, it appears likely that the mingling of the taste and reward systems occurs similarly in rodents and primates, even though the latter lacks a direct ponto-VTA-accumbens pathway: tastes activate the nucleus accumbens upon reaching the forebrain taste relays.

6.5. THE LINK BETWEEN TASTE AND REWARD ACTIVITY DRIVES BEHAVIOR

The literature reviewed thus far suggests that taste stimuli are unavoidably and intrinsically laden with reward value. This linkage is seen in the behaviors that reveal each taste’s current palatability, in the physiology of neural taste responses that intrinsically contain information concerning reward value, and in the anatomy of the taste system, which is reciprocally connected to basic reward centers in the brain. Based on such data, we suggest that tastes are, for all intents and purposes, rewards.

But perhaps the most telling evidence that tastes are rewards lies not in any particular taste data themselves, but in a meta-analysis of the use of tastes in studies of reward learning. Reward or incentive learning is currently an area of great interest in neuroscience (cf. Chapter 13). Many researchers are currently involved in studying the way in which arbitrary, otherwise neutral, stimuli become imbued with value when linked to a more intrinsically rewarding stimulus. At the most general level, these researchers seek to explain the nature of the association produced via this pairing (e.g., is it specific to the particular reward, or general to “rewardiness?”) and the involvement of the dopamine system in this process. But it all starts with placing an intrinsic reward into close temporal proximity with some arbitrary or neutral stimulus (or action).

The neutral stimuli used in primate and rodent incentive learning experiments are variously drawn from the visual, auditory, or olfactory domains, but in the vast majority of these studies, the intrinsically rewarding stimulus to which the neutral stimulus is linked is a taste—tastes are rewards for animals as diverse as monkeys and the flies that bother them. For example, when a researcher desires to imbue an otherwise neutral, innocuous olfactory stimulus with the ability to drive dopamine release in a rat, s/he delivers that odorant in close association to a sweet solution (Schoenbaum, Chiba, and Gallagher 1998; Schoenbaum 2001). This association “works” (once it is recognized by the rat) regardless of whether the sweet taste is caloric (e.g., Sheffield and Roby 1950; Dufour and Arnold 1966) and regardless of whether the animal is allowed to experience any post-ingestive effects of consuming the substance (e.g., Hull 1951). ^* It is clear, therefore, that it is the taste itself that carries reward value to be attached to the odor. Intracranial stimulation of the VTA also works well to drive reward learning (Fibiger et al. 1987; Garris et al. 1999), but the functionality of these physiologically unusual stimuli likely reflects the strong dopaminergic action of taste administration itself.

Further evidence that tastes are truly the rewards driving incentive learning to other stimuli comes from studies making use of the fact that a taste’s reward value, while intrinsic, is plastic. For instance, when a taste is quickly “devalued” (when the experimenter induces a reduction of the taste’s reward value) through either conditioned taste aversion (e.g., Colwill and Rescorla 1985) or feeding to satiation (e.g., Balleine and Dickinson 1998), associated non-taste stimuli are similarly robbed of reward value (this once again points to the importance of post-ingestive effects on calculation of reward; see Chapter 12). So effective is devaluation at interfering with the function of incentive learning mechanisms that the opposite of satiation—inducement of hunger via restriction of food access prior to training—is a nearly ubiquitous part of the preparation of rats for learning experiments.

In summary, an entire field of research involving both rodents and primates has been founded upon the intrinsic “rewardiness” of taste, or more specifically on the ease with which any non-taste stimulus that is temporally linked to a taste stimulus can gain access to the reward system via that taste. ^† This associative access to reward networks makes perfect, even inevitable, evolutionary sense: as noted in the introduction, the fact that tastes are natural rewards is inextricably linked to the fact that the activation of reward pathways by taste stimulation occurs only late in the game (assuming that the game is diet procurement), after the potentially nourishing or poisoning food has been placed into the mouth. Reward value must subsequently be transferred from the taste of the food to the sight and smell of the food if the animal is to optimize its survival odds—a distinct advantage is conferred upon the animal that is able to predict nourishment or poison while the potential food object is still external. That is, incentive learning is evolutionarily adaptive, in much the same way that conditioned taste aversions and preferences are, because it helps an animal figure out what it should eat.

6.6. RETHINKING “FLAVOR” IN THIS FRAMEWORK

Put another way, the key to making the rewarding properties of taste “useful” to an animal involves having strong connections between the taste and other sensory systems. Taste input interacts with visual, somatosensory, auditory, and above all olfactory information to optimize an animal’s success. Thus, it would be reasonable to expect that information in these other sensory systems had an impact on taste system function.

In fact, this impact is a much-studied one: it is well known that the “flavor” of a food item, while appearing to the taster to emerge from the tongue, is in fact a holistic, multi-modal perceptual construct. Each and every sensory modality appears to be involved in the construction of a flavor percept (Verhagen and Engelen 2006). Not only involved, however: flavor is the apparent enrichment and outright changing of the response to a relatively impoverished taste stimulus by these other sensory systems. While taste can modulate the intensity of olfactory and somatosensory percepts (Verhagen and Engelen 2006), the most common conclusion reached on the basis of flavor research is that taste is a relatively weak player in the determination of flavor.

But this work, which has been done in relative isolation from the research discussed in the previous section, begs the question “why does flavor exist?” Where is the survival value in the apparent taste of an object being so dependent on input from other sensory systems, when other percepts seem (at first blush, see below) to be largely determined by unimodal input? Why should stimulation of the tongue not provide a rich and reliable description of the food? If the answer is that taste information is too impoverished to identify the complex range of potential foods in the world (most believe that taste consists entirely of four or five basic qualities, see Smith and St John 1999), why then is that so? Why didn’t we evolve to have a tongue that, like our noses, is outfitted with hundreds of different receptors (Kay and Stopfer 2006), each tuned to a subtle subset of the myriad molecules that make up food? What is adaptive about the loveliness of the gourmet restaurant meal?

We propose, perhaps provocatively, and in full awareness of the burgeoning field of flavor research, that the answer may well be “nothing.” Flavor as a rich sensory experience may be a spandrel (Gould 1997), a side effect of natural selection for the deeply adaptive trait of incentive learning already described. Specifically, if the probability of survival is enhanced with proper recognition of stimuli that will ultimately reward and punish when in the mouth, such that animals benefit greatly from being able to “map” a food’s taste properties onto stimuli impinging on other sensory systems, then what is probably selected for is strong connections between taste and the other sensory systems for the purpose of driving action in response to those stimuli. Flavor could simply be something that we get “for free” from a system designed to ensure the functioning of incentive learning in natural situations.

Note that we are not suggesting that feeding, an obvious target of selective pressure, relies on taste in the absence of influence from the other senses. Diet selection is clearly more a function of olfaction and vision than of taste. A basis of the argument made here is in fact that diet selection is almost exclusively under the control of olfaction and vision—the diet is selected before the food reaches the mouth—but that the effective use of olfaction and vision for these purposes is the result of incentive learning, for which simple taste properties are the primary rewards. We are simply unaware of a strong argument as to how appropriate feeding requires flavor in a manner that cannot be more easily explained under these terms (although one possibility is that multi-sensory stimulation allows for the detection of otherwise undetectable substances, see for instance Dalton et al. [2000]). ^*

If this reasoning is correct—if the purpose of intersensory interactions involving taste is not the emergence of flavor but the transmission of reward from taste to other sensory systems—then the following prediction becomes reasonable: it should be possible, in a situation involving a rewarding non-taste stimulus, to demonstrate the same process that is evident in flavor working “in reverse,” namely, passage of this reward to a consumed taste, and modulation of perception of the originally rewarding stimulus via perturbation of the taste system. We have recently published a study confirming this prediction, using social transmission of food preference. This task takes advantage of an olfactory stimulus that for the rat appears to have intrinsic, almost taste-like, reward value: carbon disulfide (CS₂), the smell of another rat’s breath. A rat that smells a food odor mixed with CS₂ develops a preference for that food in a subsequent taste test. We first directly demonstrated that olfactory input is necessary and sufficient for proper preference development and then demonstrated the preference to be dependent on taste cortex using a temporary inactivation technique. Finally, by inactivating taste cortex during both training and testing sessions, we revealed a classic state-dependency: an odor is changed by taste cortex inactivation, such that proper recognition of that odor only occurs when taste cortex is again inactivated (Fortis-Santiago et al. 2010, Figure 6.2).

FIGURE 6.2

The taste system alters olfactory perception. The results of socially transmitted food preference tests, which rely wholly on olfactory stimulation (Fortis-Santiago et al. 2010). The left-most pair of bars show what happen when control rats are trained (more...)

6.7. CONCLUSIONS

This research makes the argument that sensory system function has not been “specialized” for flavor. The linkage between taste and olfaction is a mutual one, allowing each to take advantage of the reward information inherent in the other. Each modulates the other as a byproduct of this optimization. Likely, the relationships between taste and the other sensory systems are to at least some degree similar. None of these relationships is 100% symmetric, for reasons laid out in the first sections of this essay, but the purpose of each intersensory interaction is probably the same. In fact, this finding allows us to more easily view flavor through the general lens of multi-sensory interaction, in which such reciprocal interactions are increasingly recognized to be commonplace (Ghazanfar and Schroeder 2006). The McGurk effect, wherein the sight and sound of a speaker mutually impact perception of each other, is the most well known result of these interactions, but in the service of effective communication—another prominent source of reward—vision and audition constantly update and change each other (Ghazanfar and Hauser 1999; Ghazanfar et al. 2005; Campbell 2008).

This broader view, which follows directly from the fact that tastes are the only stimuli that must be ingested to be sensed, has the power to change the way we think about, and do research studying, flavor. It suggests, for example, that we would be well advised to not look for circuitry that is dedicated to the production of flavor percepts, nor to think of flavor as a “one-way street” toward rich perceptual experience. At the most general level, this essay puts the study of taste and affiliated stimulus attributes into a more Gibsonian framework (Gibson 1966, 1982), in which the multi-modal flux of incoming stimulation is mined to reveal the important intrinsic properties of food objects in the environment; in this framework, the purpose of sensory input is to drive action toward such objects. The “flavor” of these objects is secondary to the divination of whether they afford consumption—an affordance that is directly ascertained through their taste attributes (which signal reward), and re-mapped to their visual, olfactory, auditory, and somatosensory attributes.

ACKNOWLEDGMENTS

The time spent musing on these issues was generously funded by the NIDCD (grants DC 006666 and DC 007102) and the Swartz Foundation. We are deeply indebted to the members of the Katz lab and Asif Ghazanfar for endless discussions, and to Dana Small for a little text and a lot of tolerance.

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Footnotes

*

This is not to deny the reality of post-ingestive effects, which are a necessary and important consequence of a taste object’s access to the digestive system. While data summarized in this chapter demonstrate that tastes have reward value in the absence of either experience or post-ingestive effects, it remains likely that taste becomes synonymous with reward only via “learning” about the post-ingestive effects of eating that occurred across evolutionary time (and, in certain circumstances, early in post-natal life, see Changizi, McGehee, and Hall 2002).

*

The data alluded to in this paragraph form the substrate for the most heated debate in taste science. Researchers who focus on the function of taste receptor cells (Scott 2004), or who are impressed by narrowly tuned brainstem neurons (Frank 2000), favor a “labeled line” theory of coding, whereby tastes are identified via activation of specific subsets of highly responsive neurons (e.g., “sucrose-best neurons”). Researchers who focus on output cells in the taste buds (Roper and Chaudhari 2009), or who are impressed by broadly tuned brainstem neurons (Lemon and Katz 2007), instead argue an “across-neuron pattern” theory, whereby tastes are identified via decoding of the pattern of activation across responding and non-responding neurons.

*

Although, as discussed by de Araujo in this volume, the long-term maintenance of taste-reinforced associations may require the use of caloric, energy-rich tastes that elicit post-ingestive effects.

†

Of course, the mere fact that taste research has been founded on taste “rewardiness” is not iron-clad proof of taste rewardiness; for much of history, a great deal of otherwise rigorous physics research was founded on the mistaken idea that the Earth is the center of the universe.

*

Part of the attractiveness of this characterization lies in the fact that it also provides a simple, parsimonious explanation for the mysterious impoverishment of taste itself—i.e., the fact that the tongue seems to come equipped to detect only combinations of four to five tastes: if complex flavor perception isn’t the raison d’etre of the system, then there was no selective pressure to increase the complexity of the input.