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Murray MM, Wallace MT, editors. The Neural Bases of Multisensory Processes. Boca Raton (FL): CRC Press/Taylor & Francis; 2012.

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Chapter 36A Proposed Model of a Flavor Modality

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36.1. INTRODUCTION

The perception of flavor occurs when a food or drink enters the mouth. Although the resulting perception depends on inputs from multiple sensory modalities, it is experienced as a unitary percept of a food or beverage. In this chapter the psychophysical characteristics and neural substrates of flavor perception are reviewed within the context of a proposed model of a flavor modality in which the diverse sensory inputs from the mouth and nose become integrated. More specifically, it is argued that a binding mechanism in the somatomotor mouth area of the cortex brings taste, touch, and smell together into a common spatial register and facilitates their perception as a coherent “flavor object.” We propose that the neural representation of the flavor object is a distributed pattern of activity across the insula, overlying operculum (including the somatomotor mouth region), orbitofrontal, piriform, and anterior cingulate cortex.

36.2. FLAVOR IS TASTE, TOUCH, AND SMELL

When we “taste,” we also touch the food or drink in our mouths and sense its odor, via retronasal olfaction (Figure 36.1). The term flavor describes this multimodal experience. The gustatory sense (i.e., taste) refers specifically to the sensations of sweet, sour, salty, bitter, savory (Bartoshuk 1991; Chandrashekar et al. 2006), and perhaps fat (Chale-Rush et al. 2007; Gilbertson 1998; Gilbertson et al. 1997). Each of the five major taste qualities serves to signal a specific class of nutrients or potential threats: sweet signals energy in the form of calories, salty signals electrolytes, sour signals low pH, savory (umami) signals proteins, and since most poisonous substances are bitter, bitterness signals potential toxins (Scott and Plata-Salaman 1991). Thus, the sense of taste helps identify physiologically beneficial nutrients and potentially harmful stimuli. Because taste receptors lie side by side in the oral cavity with thermoreceptors, mechanoreceptors, and nociceptors, everything that is tasted induces tactile and thermal sensations, and sometimes also chemesthetic sensations (e.g., burning and stinging; Green 2003; Simon et al. 2008). In addition, some taste stimuli can themselves evoke somatosensory sensations. For example, in moderate to high concentrations, salts and acids can provoke chemesthetic sensations of burning, stinging, or pricking (Green and Gelhard 1989; Green and Lawless 1991). Consequently, even presumably “pure taste” stimuli can have an oral somatosensory component.

FIGURE 36.1. Orthonasal vs.

FIGURE 36.1

Orthonasal vs. retronasal olfaction. Schematic depiction of two routes of olfactory perception: orthonasal and retronasal. Odors sensed orthonasally enter the body through the nose (nares) and travel directly to olfactory epithelium in nasal cavity. Odors (more...)

The taste signal itself is carried from taste receptor cells in the oral cavity by cranial nerves VII, IX, and X to the nucleus of the solitary tract in the brainstem, where taste inputs are joined by oral somatosensory projections from the spinal trigeminal nucleus. The precise locations of the trigeminal projections vary across species, but there is evidence (including in humans) of overlap with gustatory areas (Whitehead 1990; Whitehead and Frank 1983), and of tracts that run within the nucleus of the solitary tract that may facilitate cross-modal integration (Travers 1988; Figure 36.2). Somatosensory input also reaches the nucleus of the solitary tract via the glossopharyngeal nerve, which contains taste-sensitive, as well as mechano- and thermosensitive neurons (Bradley et al. 1992). Overlapping representation of gustatory and somatosensory information also occurs in the thalamus (Pritchard et al. 1989) and at the cortical level (Cerf-Ducastel et al. 2001; Pritchard et al. 1986). For example, the primary gustatory cortex contains nearly as many somatosensory-specific as taste-specific neurons, in addition to bimodal neurons responding to both somatosensory and taste stimulation (Kadohisa et al. 2004; Plata-Salaman et al. 1992, 1996; Smith-Swintosky et al. 1991; Yamamoto et al. 1985). In sum, taste and oral somatosensation have distinct receptor mechanisms, but their signals converge at virtually every level of the neuroaxis, suggestive of extensive interaction.

FIGURE 36.2. Oral sensory pathways.

FIGURE 36.2

Oral sensory pathways. A glass brain schematic depiction of taste (black circles), somatosensory (white circles), and olfactory (gray circles) pathways. Anatomical locations are only approximate and connectivity is not exhaustive. Information from taste (more...)

Although taste and oral somesthesis provide critical information about the physicochemical nature of ingested stimuli, it is the olfactory component of food that is required for flavor identification (Mozell et al. 1969). The acts of chewing and swallowing release volatile molecules into the oral cavity, which during exhalation traverse the epipharynx (also referred to as the nasopharynx) and stimulate receptors on the olfactory epithelium. This process is referred to as retronasal olfaction (Figure 36.1), in contrast to orthonasal olfaction, which occurs during inhalation through the nose. Both orthonasal and retronasal olfactory signals are carried via cranial nerve I to the olfactory bulb, which projects to the anterior olfactory nucleus, the olfactory tubercle, the piriform cortex, several amygdaloid subnuclei, and rostral entorhinal cortex and thalamus. These areas, in turn, project to additional amygdala subnuclei, the entorhinal, insula, and orbitofrontal cortex (OFC) (de Olmos et al. 1978; Price 1973; Turner et al. 1978; Figure 36.2). Thus, olfactory information is carried to the brain by distinct pathways and does not converge with gustation and oral somatosensation until higher-order cortical regions, such as the insula and the OFC.

In summary, the perception of flavor depends on multiple distinct inputs that interact at several levels in the central nervous system. How these interactions act to “bind” the signals into coherent perceptions of flavor is currently unknown. Here, we propose a model in which the somatomotor mouth area orchestrates this binding via a process that results in referral of olfactory sensations to the oral cavity. It is worth noting that flavor percepts can also be influenced by visual inputs (Koza et al. 2005) and by beliefs and expectations (de Araujo et al. 2003), which are factors that represent top-down modulation of flavor. However, these types of cognitive effects are outside the scope of the present chapter.

36.3. ORAL REFERRAL

Consistent with the concept of “proximity” proposed by Gestalt psychologists (Kohler 1929), it is well known that stimuli that appear to originate from a common location are interpreted as having a common source (Stein 1998). In the case of flavor, sensory mechanisms exist that cause all of the perceptual components of flavor (taste, smell, and touch) to appear to arise from the oral cavity (Green 2003; Hollingworth and Poffenberger 1917; Lim and Green 2008; Murphy et al. 1977; Prescott 1999; Small and Prescott 2005; Todrank and Bartoshuk 1991). Here we argue that the function of these referral mechanisms is to bring the sensory components of flavor into a common spatial register that facilitate their binding into a “flavor object.” This process may also be aided by the fact that odors and tastes can share common sensory characteristics (e.g., some odors are perceived as sweet) that blur the qualitative boundary between taste and smell and facilitate integration (Auvray and Spence 2008).

Although several authors have proposed the existence of an object-based flavor system (Auvray and Spence 2008; Green 2003; Prescott 1999; Small 2008; Small and Prescott 2005), the neuro-physiology of the hypothesized system remains relatively unexplored. The model proposed here holds that oral referral is required for the perception of flavor objects, and neural mechanisms that mediate referral and flavor learning are posited. Because oral referral is central to the model, we begin our discussion with the various forms of referral that have been described.

36.3.1. Olfactory Referral

As noted above there are two ways to smell: during inhalation through the nose (orthonasal olfaction) and during exhalation through the mouth (retronasal olfaction) (Figure 36.1). Orthonasally sensed odors appear to emanate from objects in the external world, whereas retronasally sensed odors often appear to emanate from the oral cavity (Heilmann and Hummel 2004; Hummel et al. 2006; Murphy et al. 1977; Rozin 1982) and may be confused with taste (Ashkenazi and Marks 2004; Hollingworth and Poffenberger 1917; Murphy et al. 1977; Murphy and Cain 1980). Although scientists have been aware of the misattribution of smell as taste for some time (Tichener 1909), the first systematic study was made by Murphy et al. (1977). In that study, Murphy and her colleagues investigated the nature of taste–odor interactions by asking subjects to estimate the intensity of tastes, odors, and their mixtures. The results showed that the perceived intensity of a taste–odor mixture roughly equalled the sum of the perceived intensities of the unmixed components, indicating that tastes and odors were perceptually independent. However, subjects attribute approximately 80% of the mixture’s intensity to the gustatory modality (Murphy et al. 1977). Specifically, taste intensity ratings were higher when the nostrils were open compared to when they were pinched (a stylized version of this finding is represented in Figure 36.3). Since the odor they used, ethyl butyrate, smells sweet, they suggested the effect resulted from a combination of shared sensory properties (sweet) and the misattribution of the retronasal olfactory sweet component to the taste system due to the referral of the odor to the oral cavity. This and subsequent studies also ruled out the possibility that referral could be attributed to the activation of taste cells by odors, because the chemicals that produce taste-like smells (e.g., strawberry smells sweet) do not taste sweet when sampled in the mouth with the nares occluded (Murphy and Cain 1980; Sakai et al. 2001; Schifferstein and Verlegh 1996; Stevenson et al. 2000b). Thus, the sweet quality of an odor occurs in the absence of the activation of taste receptor cells, but when sensed retronasally may nevertheless be attributed to taste.

FIGURE 36.3. Taste–odor confusion.

FIGURE 36.3

Taste–odor confusion. This figure is a stylized representation of data reported in Figure 4 of Murphy and colleagues (1977) (rendered with permission from Dr. Claire Murphy) and represents first experimental demonstration of taste–odor (more...)

Indeed, it has been argued that orthonasal and retronasal olfaction represent two distinct modalities. Inspired by a comment made by a friend that “I really love the taste (of Limburger cheese) if only I can get it by my nose,” Rozin (1982) first proposed that olfaction is a dual-sense modality, with one component (orthonasal olfaction) specialized for sensing objects in the world and the other (retronasal olfaction) specialized for sensing objects in the mouth. Building upon Gibson’s proposal that “tasting” and “smelling” are distinct perceptual systems that cut across receptor classes, Rozin suggested that “the same olfactory stimulation may be perceived and evaluated in two qualitatively different ways, depending on whether it was referred to the mouth or the external world.” In support of this view, he found that subjects frequently reported disliking the smell, but liking the taste, of certain foods (e.g., fish, eggs, and cheese). He also demonstrated that subjects had great difficulty correctly identifying flavor stimuli that had first been learned via the orthonasal route. These data are therefore consistent with the notion that olfactory stimuli arising from the mouth have different sensory–perceptual properties than those originating in the external world. Rozin suggested that these perceptual processes might be achieved by differential gating of inputs triggered by the presence of a palpable object in the mouth, or by the direction of movement of the odor across the olfactory mucosa. Alternatively, he posited that it may be that odor information is not gated but rather is combined with available oral inputs into an emergent percept in which the olfactory component loses its separate identity.

After the publication of Rozin’s hypothesis, several investigators argued that the differences between orthonasal and retronasal olfaction were primarily quantitative rather than qualitative. This argument was based on evidence that retronasal stimulation by the same physical stimulus tends to result in lower perceived intensity than orthonasal stimulation (Pierce and Halpern 1996; Voirol and Dagnet 1986). Although it is clear that quantitative differences are present, there is also more recent evidence supporting the duality hypothesis (Bender et al. 2009; Heilmann and Hummel 2001; Hummel et al. 2006; Koza et al. 2005; Landis et al. 2005; Small et al. 2005; Sun and Halpern 2005; Welge-Lussen et al. 2009). Of particular note, Hummel and his colleagues devised a method for delivering odorants in the vapor phase via either the ortho- or retronasal routes (Figure 36.4). Critically, the method allows assessment of retronasal olfaction without stimulation of the oral cavity (Heilmann and Hummel 2004). Two tubes are inserted into the subject’s nose under endoscopic guidance so that one tube ends at the external nares (to achieve orthonasal delivery) and the other tube at the epipharynx (to achieve retronasal delivery). The tubes are, in turn, connected to a computer-controlled olfactometer that delivers pulses of odorant embedded in an odorless airstream. Using an electronic nose to measure the stimulus in the airspace below the olfactory epithelium, the authors demonstrated that the maximum concentration and duration of the signal was equivalent after delivery by either route (Hummel et al. 2006). Despite similar signals and the absence of oral stimulation, the olfactory localization illusion was, in part, maintained (Figure 36.5). Subjects were more likely to report that the retronasal odors came from the back of the throat, whereas orthonasal odors appeared to come from the nose. The mechanism(s) behind the olfactory referral illusion remain unknown. However, this study ruled out intensity differences as a cue, because the odors were titrated to equate perceived intensity. The finding also suggests that oral stimulation is not required for at least some referral to occur, since the procedure involved neither a gustatory nor somatosensory stimulus. However, in a subsequent investigation in which subjects were asked to indicate if the odor were delivered orthonasally or retronasally (rather than localize it to the nose or mouth), trigeminal (chemesthetic) stimulation was found to be an important factor for making the discrimination (Frasnelli et al. 2008). More work is therefore needed to determine the degree to which odors can be referred to the mouth based on the direction of flow of the olfactory stimulus.

FIGURE 36.4. (See color insert.

FIGURE 36.4

(See color insert.) An MRI image showing tubing placement using methods described by Heilmann and Hummel (2004). This sagittal brain section reveals placement of nasal cannulae at external nares to achieve orthonasal delivery, and at nasopharynx to achieve (more...)

FIGURE 36.5. Odorant localization.

FIGURE 36.5

Odorant localization. Preliminary data from 20 subjects showing that orthonasal odor is perceived as coming from front of nasal cavity and retronasal odor as coming from back of nasal/oral cavity (throat). This perception occurred despite constant airflow (more...)

A possible mechanism by which such referral might occur is the direction of odorant flow across the olfactory epithelium. Indeed, since the data supplied from the electronic nose indicated that the physical stimulus arriving at the epithelium can be identical (at least for the measured parameters), the primary difference between the routes in Hummel’s experiments was the direction of odorant flow. Hummel and colleagues therefore suggested there may be a distinct organization of olfactory receptor neurons in the back versus the more anterior portions of the nasal cavity. This hypothesis is consistent with Mozell’s chromotagraphic model of olfaction, which postulates that the pattern of odorant binding to receptors can lead to different odor perceptions (Mozell 1970). Further support for the chromatographic model comes from a study in the laboratory of Sobel et al. (1999), which showed that subtle differences in airflow patterns between the left and right nostrils can lead to different perceptual experiences.

Although neither taste nor oral somatosensation appear to be required for at least some degree of referral to occur (Heilmann and Hummel 2004; Hummel et al. 2006; Small et al. 2005), further study is needed to determine if stimulation of these modalities may nevertheless contribute to referral.

In summary, the olfactory localization illusion, coupled with the fact that flavor identity is conveyed primarily by olfaction, leads to the perception that flavors come from the mouth. Despite the fact that this illusion has a profound impact on flavor perception, the mechanisms that produce it remain unknown. Possible mechanisms include spatiotemporal differences in odorant binding across the olfactory epithelium during retro- versus orthonasal stimulation, and/or capture by tactile and/or gustatory stimulation.

36.3.2. Taste Referral: Localization of Taste by Touch

Not only are retronasal odor sensations referred to the mouth and attributed to taste; taste sensations can be referred to the location of tactile stimulation on the tongue (Green 2003; Lim and Green 2008; Todrank and Bartoshuk 1991; Figure 36.6). This illusion was first demonstrated by Todrank and Bartoshuk (1991), who were motivated by the observation that during eating, taste sensations seem to originate throughout the tongue even though the taste buds are located at specific loci (tip, side, and back of the tongue and soft palate). The authors postulated that this effect might depend on a capture-illusion similar to the ventriloquist effect, whereby one sensory modality dominates the other (Tastevin 1937). Specifically, it was hypothesized that taste localization is dominated by touch in a manner akin to the phenomenon of thermal referral (Green 1977), in which touch dominates localization of thermal sensation. To test this prediction, Todrank and Bartoshuk asked subjects to report the intensity of taste as a stimulus was painted onto the tongue along a path that traversed regions of high and low taste bud density. When the path began in a region of low taste bud density, taste sensations started out weak. As the path intersected regions of greater taste bud density, taste sensations became stronger. However, when the path returned to low density regions the sensation remained nearly as intense as it was in the high density region. The authors interpreted this result to mean that the taste sensation was “captured” by the tactile stimulation of the swab and dragged into the insensitive area. More recent work has corroborated this interpretation by finding that tastes can be localized to a spatially adjacent tactile stimulus (Green 2003; Lim and Green 2008; Figure 36.6).

FIGURE 36.6. Taste localization by touch.

FIGURE 36.6

Taste localization by touch. Stimulus configuration used to measure referral of taste sensations to site of tactile stimulation. On each trial, experimenter touched three saturated cotton swabs simultaneously to anterior edge of tongue, producing identical tactile (more...)

Although it is also true that tastes can be localized independently from touch (Delwiche et al. 2000; Lim and Green 2008; Shikata et al. 2000), we believe that referral of taste to touch helps to create a coherent “perceptive field” onto which odors are also referred, thus providing the foundation for a unitary flavor percept.

36.3.3. Shared Qualities between Olfaction and Taste

In addition to oral referral mechanisms, shared qualities between olfaction and taste promote the integration of tastes and smells in flavors. Odors often have taste-like characteristics (Dravnieks 1985; Harper et al. 1968), which may be acquired by experience (Stevenson 2001; Stevenson and Boakes 2004; Stevenson et al. 2000a; Stevenson and Prescott 1995; Stevenson et al. 1999). It has been proposed that the existence of these shared qualities, coupled with olfactory referral, blurs the boundary between taste and smell, which in turn facilitates the sensation of a unitary percept (Auvray and Spence 2008; McBurney 1986).

In summary, there are at least three mechanisms that promote the integration of discrete sensory inputs that are stimulated during feeding and drinking into a unitary flavor percept or object: olfactory referral, taste referral to touch, and shared taste–odor qualities.

36.4. THE PROPOSED MODEL

The central tenant of the proposed model is that oral referral mechanisms play a critical role in encoding flavor by helping to fuse multisensory inputs into a perceptual gestalt. This idea builds upon, and has direct parallels with, the coding of “odor objects” as described by Haberly (2001) and by Wilson and Stevenson (2003), and “odor–taste learning” described by Stevenson and Boakes (2004). Therefore, a brief discussion of odor objects follows.

36.4.1. Odor Objects

Wilson and Stevenson (2003) suggest that although the peripheral olfactory system may be organized to emphasize analytical processing (Buck and Axel 1991), the primary function of olfactory cortex is the experience-dependent synthesis of odorant components into unique, identifiable odor objects. Critically, the neural representation of the odor object is distinct from the representation of its sensory components, and it is the encoding of the entire pattern of activity that forms a perceptual gestalt. Wilson and Stevenson base this argument on what they view as two cardinal features of olfactory perception: that it is (1) synthetic and (2) experience-bound.

36.4.1.1. Synthesis

With regard to synthesis, Wilson and Stevenson (2003) propose that odor elements combine to produce novel odor qualities within which the odor elements are no longer discernible, and thus that olfaction is a synthetic modality akin to color vision. Recognizing that these perceptual features of olfaction are at odds with the analytical organization of the peripheral olfactory system, Wilson and Stevenson argued that an experience-dependent synthesis of odor information from the periphery occurs (Haberly 2001) that creates an emergent neural code in the cortex. Specifically, they proposed that neurons in anterior piriform cortex receive signals about odorant features from the olfactory bulb (analytical elements) and initially function as coincident feature detectors (Figure 36.7). The response properties of the cortical neurons then rapidly shift as stimulation continues, resulting in an experience- and odorant-dependent neural signature within an ensemble of neurons, the “odor object.” In support of this view, recent work from Wilson’s laboratory examined neural and perceptual responses to a set of odorant mixture “morphs”—odor mixtures with one or more components of a 10-component (stock) mixture either removed or replaced (Barnes et al. 2008). Electrohphysiological recordings from the rodent brain showed that the neural ensemble activity in the piriform cortex, but not in the olfactory bulb, remained correlated when one of the components was missing, resulting in rats being unable to discriminate the nine-element mixture from the stock mixture. However, when a component was replaced, the piriform ensemble activity decorrelated and discrimination was possible. This suggests that neural ensembles in rodent piriform cortex code odor quality and perform pattern completion to support perceptual stability of odor objects. Similarly, in humans, Gottfried and colleagues used functional magnetic resonance imaging (fMRI) to demonstrate a double dissociation of odor coding in the piriform cortex, with the posterior piriform sensitive to the physiochemical features of odors (i.e., alcohol vs. aldehyde) and not the odor quality (e.g., vegetable vs. fruit), and the anterior piriform sensitive to odor quality and not physiochemical features (Gottfried et al. 2006b). This result indicates that it is the odor object, and not the physical stimulus, that is represented past the initial cortical relay. Since it is likely that conscious perception of odors in humans requires the OFC (Li et al. 2008), it is reasonable to conclude that olfactory perceptions are based on odor objects.

FIGURE 36.7. (See color insert.

FIGURE 36.7

(See color insert.) Synthetic processing in anterior piriform cortex. This figure depicts model of olfactory processing proposed by Wilson and Stevenson. Recent olfactory sensory physiology is consistent with a view of olfactory bulb mitral cells serving (more...)

However, the development of unique neural codes representing odors and odor mixtures does not necessarily mean that odor objects are perceptually synthetic. Although studies of odor identification in mixtures by Laing et al. (Laing and Francis 1989; Livermore and Laing 1996) have been cited as evidence of synthesis (Wilson and Stevenson 2003), those results actually show a degree of analytical processing that led Livermore and Laing (1996) to conclude that “… olfaction is neither entirely analytic nor synthetic, but … contains elements of both” (p. 275). Thus, even though both “expert” and novice subjects have difficulty identifying more than two or three odors in a mixture (Livermore and Laing 1996), the ability to perceive at least some components rules out a purely synthetic process. We therefore favor the view of Jinks and Laing (2001) that olfactory perception is “configurational” in a manner similar to facial perception in vision (Rakover and Teucher 1997). As those authors described it, configurational processing is based on perceptual fusion rather than perceptual synthesis of odor qualities, which creates a gestalt in which “limited analysis” of mixture components is possible. This view is also consistent with Gottfried’s conclusion that emerging data in olfactory neuroscience support the conclusion “that the brain has simultaneous access to the elemental and configural representations” (Gottfried 2009). As will be shown below, this concept has also been applied to flavor perception.

36.4.1.2. Experience

There are many examples of experience dependence in the olfactory system (Dade et al. 1998; Dalton et al. 2002; Li et al. 2006; Wilson et al. 2006). One particularly elegant example of olfactory perceptual learning comes from Li and colleagues, who presented subjects with odor enantiomer pairs (mirror image molecules) that were initially indistinguishable (Li et al. 2008). Subsequently, they associated one member of the enantiomer pair with a shock. This resulted in perceptual learning in which subjects became able to distinguish the members of the pair and, consistent with Wilson and Stevenson’s theory, this was accompanied by a divergence in neural response to the odor pair in the anterior piriform cortex.

A second example of the role of experience in shaping olfactory perception, which is particularly relevant to this chapter, is that when an odor is experienced with a taste, the odor later comes to smell more like the taste with which it was experienced (Stevenson and Prescott 1995). This has been termed the acquisition of taste-like properties by odors, and is described in depth in Chapter 35 by Prescott. It is likely that this form of perceptual learning plays an important role in the formation of the flavor objects.

36.4.2. Flavor Objects

As noted above, flavor perception has been described as resulting from a process of sensory fusion (Auvray and Spence 2008; McBurney 1986). One can introspect and identify the olfactory component of a flavor (e.g., strawberry) as well as the taste component of a flavor (sweet and sour); however, since some percepts (sweet) are communal, the boundary between what is odor and what is taste is not always discernible. Thus, consistent with our view of odor objects, we propose that the elements of flavor are discernible yet fused. Unlike olfaction, which may promote configural processes, taste appears to be primarily analytic (Breslin 2000); tastes do not mix to produce novel percepts. Flavor percepts therefore arise from the binding of neural processing in a distributed pattern of distinct elements that maintain their individual quality to varying degrees (e.g., tastes more so than odor objects). In addition, there is evidence that the response selectivity of bimodal (odor- and taste-sensitive) neurons is shaped by the coactivation of unimodal inputs (Rolls 2007). It is therefore proposed that, like the creation of odor objects, the creation of flavor objects depends on a distributed pattern of neural activity that is sculpted by experience.

What might this pattern of neural activity look like? It is argued that that it is a distributed circuit including the neural representation of the odor object, unimodal taste cells, unimodal oral somatosensory cells, multimodal cells, and a “binding mechanism” (Figure 36.9). We propose that it is the activation of the binding mechanism that mediates oral referral, and that the binding mechanism is required to fuse flavor components into a flavor object. As such, retronasal olfaction has a privileged role in the formation of flavor objects. That is, unless a flavor has been experienced retronasally, it is not incorporated into a flavor object. A prediction that follows from this line of reasoning is that if Stevenson’s basic, taste–odor learning paradigm is repeated, but the conditioning trials are performed with orthonasal rather than retronasal odor stimulation, then the odors should not acquire taste-like properties. This experiment has yet to be carried out.

FIGURE 36.9. Proposed flavor network.

FIGURE 36.9

Proposed flavor network. A “glass” brain drawing depicting proposed flavor network as gray circles. G, gustation; S, somatosensation; O, olfaction. Arrows indicate point of entry for sensory signal. Dashed line box with GS represents gustatory (G) (more...)

36.4.3. Encoding of Flavor Objects

Upon binding of the associated distributed responses, a flavor object is created and must be encoded in memory. Although it is clear that the interaction between tastes and odors is experience-dependent, the nature of the learning is currently unknown. There are several possibilities. First, odor objects, consisting of the activity of unimodal olfactory cells, could—via associative learning—come to acquire the ability to activate taste cells (Rescorla 1981). In this case, the connection between a unimodal taste-responsive neuron and a unimodal smell-responsive neuron that fire together is strengthened, so that the experience of the odor alone is able to cause the taste-responsive neuron to fire. Based on perception, it is clear that this process would have to be asymmetrical, because although some odors have taste-like characteristics, no tastes have odor-like characteristics. Such an organization is unlikely because bimodal taste–odor neurons with congruent response profiles have been identified, and clearly play a role in flavor processing (Rolls and Baylis 1994). A more likely mechanism would therefore be Hebbian learning (Cruikshank and Weinberger 1996; Hebb 1949), by which odors would acquire the ability to selectively activate bimodal neurons that are simultaneously stimulated by taste cells. This type of model has been proposed by Rolls, who argues that unimodal inputs shape bimodal and multimodal cells by experience, and that the perception of flavor is encoded by the bimodal cells (Rolls et al. 1996). However, a fundamental problem with this model is that bimodal taste–odor neurons (with congruent responses to odors and tastes) fire in response to presentation of unimodal odors and unimodal tastes (Rolls and Baylis 1994), yet the perception of flavor only occurs in response to odors.

The only mechanism that can reconcile flavor perception with the known physiology is one in which the multimodal inputs from the oral cavity are encoded together as a flavor object via configural learning (Stevenson et al. 2000a,2000b). This is not to say that associative learning does not occur in the flavor modality, as it clearly does (Yeomans et al. 2006). Rather, the argument is that the initial encoding of the flavor object proceeds via configural learning. In contrast to associative and Hebbian learning, which are based on strengthening of connections of elements, configural learning involves the encoding of the entire pattern of stimulation (Pearce 2002). In other words, when a mixture is sampled by mouth, a unitary flavor is perceived rather than independent tastes and odors, and it is this unitary percept that is encoded in memory.

The empirical foundation for the assertion that the encoding of flavor objects requires configural processes comes from evidence that the enhancement of taste-like properties by odors is highly resistant to extinction and counterconditioning (Harris et al. 2004; Stevenson et al. 2000a,2000b). If odor–taste exposures strengthen the ability to activate a sensory representation of the taste (as would be the case if associative mechanisms were at play), then repeated exposure to the odor without the taste should lead to the extinction of this association (Rescorla 1981; Rescorla and Freeberg 1978), which does not occur. Counterconditioning is the process by which the association between A and B is replaced by a new association between A and C. For example, in the first phase of the experiment a subject learns that a cue “A” is associated with receipt of food “B”. Once this association is established (e.g., seeing A causes salivation), A is then paired with a new consequence that opposes B (e.g., shock). Some stimuli, such as faces, are resistant to extinction but will display counterconditioning (Baeyens et al. 1989). Stevenson and colleagues reasoned that if the acquisition of taste-like properties by odors is based on configural encoding, counterconditioning should not be possible (Stevenson et al. 2000a). To test this possibility they subjected tastes, and odors and tastes and colors, to a counterconditioning paradigm. In a single conditioning session, subjects were exposed to taste–odor and taste–color pairs. At least 24 h later, one taste–odor and one taste–color pair underwent counterconditioning (e.g., the odor and the color were paired with new tastes). As predicted, the odor maintained its original taste and did not acquire the new taste. In contrast, an expectancy measure indicated that subjects expected the colored solution to taste like the counter-conditioned taste rather than the originally conditioned taste. One caveat is that, to date, all of the odors used in studies of odor acquisition of taste-like qualities have been rated as having perceptible amounts of the target taste quality before the conditioning trials. Accordingly, it may be more accurate to view the effect of taste–odor learning as an enhancement rather than an acquisition of taste-like qualities. If so, it would not be surprising if pairing odors with other tastes failed to eliminate a taste quality that the odor possessed before the original odor–taste pairing.

An obvious next question concerns the nature of odor–somatosensory learning. There are some data to suggest that odors may acquire fat sensations after pairing with a fat-containing milk (Sundqvist et al. 2006). However, fat may be sensed via taste channels (Gilbertson 1998; Gilbertson et al. 1997), and therefore may be perceived as qualities of odors via the same mechanism as other taste qualities. Certainly, sniffed odors do not appear to invoke sensations of texture and temperature. It is likely, therefore, that although configural and synthetic processes may occur during taste–odor perceptual learning, oral somatosensory contributions to the unitary flavor percept may not be learned, and undergo sensory fusion rather than synthesis.

Notably, whereas a pure strawberry odor may result in the perception of sweetness, a pure sweet solution, or the texture of a berry, never evokes the perception of strawberry. Together with referral, these observations further support the view that olfaction has a privileged role in the flavor modality. Specifically, food identity, and thus perception of flavor objects, depends primarily on the olfactory channel (Mozell et al. 1969). Although many different foods can be characterized as predominantly sweet, predominantly salty, smooth, or crunchy, in nature there is only one food that is predominantly “strawberry” and one food that is predominantly “peach.” Such an arrangement has clear advantages because it enables organisms to learn to identify many different potential food sources and to associate them with the presence of nutrients (e.g., sugars) or toxins. Moreover, the duality of the olfactory modality allows key sensory signals about the sources of nutrients or toxins to be incorporated into the odor percept during eating and drinking (retronasal olfaction), which then enables them to be sensed at a distance (orthonasal olfaction). Indeed, although humans do not normally use their noses to sniff out food sources, the ability to use orthonasal olfaction to locate a food source is preserved (Porter et al. 2007).

36.5. NEURAL MECHANISMS

36.5.1. The Binding Mechanism

According to the proposed model, a neural substrate that orchestrates perceptual binding should exist. Since we propose that binding depends on referral, the substrate should be selectively responsive to retronasal odors. Also, activation of the binding mechanism should be independent of experience, but necessary for configurational learning to take place. Although there is no direct evidence for a region that causes or controls such processes, there is evidence that such a mechanism might exist in the somatomotor mouth area of the cortex. This evidence comes from an fMRI study investigating the effect of odorant route (ortho- vs. retro-) on evoked neural responses (Small et al. 2005). In brief, four odors were presented to subjects orthonasally and retronasally according to the procedure devised by Heilman and Hummel described above, while subjects underwent fMRI scanning. Three of these odors were nonfood odors (lavender, farnesol, and butanol), and one was a food odor (chocolate). When the responses associated with orthonasal delivery were compared to responses associated with retronasal delivery (and vice versa), there was very little differential neural response if responses were collapsed across odorant type. The only significant finding was that the oral somatomotor mouth area responded preferentially to retronasal compared to orthonasal odors, regardless of odor identity (Figure 36.8). The response in this region was therefore suggested to reflect olfactory referral to the oral cavity, which was documented to occur during retronasal, but not orthonasal, stimulation.

FIGURE 36.8. Preferential activation of somatomotor mouth area by retronasal compared to orthonasal sensation of odors.

FIGURE 36.8

Preferential activation of somatomotor mouth area by retronasal compared to orthonasal sensation of odors. Functional magnetic resonance imaging data from a study (Small et al. 2005) using the Heilmann and Hummel (2004) method of odorant presentation (more...)

It is not possible to know from this study whether the response in the somatomotor mouth area was the result or the cause of referral. However, there are several factors that point to this region as the likely locus of the binding mechanism. First, the somatomotor mouth region was the only area to show a significant differential response to retronasal compared to orthonasal stimulation. Second, responses there were independent of whether the odor represented a food or a nonfood stimulus. Third, the perception of flavor consistently results in greater responses in this region than does the perception of a tasteless solution. (Cerf-Ducastel and Murphy 2001; de Araujo and Rolls 2004; Marciani et al. 2006), indicating that it is active when flavor percepts are experienced. Fourth, since it is argued that stimulus integration and configural encoding are dependent on oral referral, it follows that the binding mechanism should be localized in the cortical representation of the mouth. We also note that the location of the binding mechanism in the somatomotor mouth area is consistent with Auvery and Spence’s suggestion that the formation of the flavor perceptual modality is dependent on a higher-order cortical binding mechanism (Auvray and Spence 2008). In addition to the initial binding, it is further predicted that neural computations in the somatomotor mouth area play a “permissive” role in enabling the sculpting of multimodal neurons. Specifically, it is proposed that unimodal taste and unimodal smell neurons located in the piriform and anterior dorsal insula sculpt the profiles of bimodal taste/smell neurons located in the ventral anterior insula and the caudal OFC only when there is concurrent activation of the binding substrate (and associated oral referral).

This model is consistent with the observations of subthreshold taste–odor summation. Whereas subthreshold summation between orthonasally sensed odor and taste appears, like taste enhancement, to be dependent on perceptual congruency (Dalton et al. 2000), subthreshold summation between retronasally sensed odors and tastes occurs for both congruent and incongruent pairs (Delwiche and Heffelfinger 2005). This suggests that experience is not required for summation of subthreshold taste and retronasal olfactory signals. This observation is consistent with the proposed model because all retronasal odors are predicted to give rise to a response in the somatomotor mouth area. In contrast, orthonasal olfactory experiences do not activate the somatomotor mouth area and are therefore not referred to the mouth. As a result, orthonasal olfactory inputs can only integrate with other oral sensations by reactivating odor objects, which have been previously associated with flavor objects.

The role of the somatomotor mouth area in oral referral and in the creation of the flavor modality could be tested in a variety of ways. For example, one could record single-unit responses in the somatomotor mouth area and the OFC in a taste–odor learning paradigm. In humans, one could examine taste–odor learning in patients with specific damage to the somatomotor mouth region or in healthy controls by using transcranial magnetic stimulation to induce temporary “lesions.” The prediction in both cases would be that lesions disrupt oral referral and the enhancement of taste-like properties by odors. Another possibility would be to use a combination of fMRI and network connectivity models such as dynamic causal modeling (Friston et al. 2003; Friston and Price 2001) to test whether response in the somatomotor mouth area to flavors influences responses in regions such as the OFC, and to test whether the magnitude of this influence changes as a function of learning.

36.5.2. Neural Correlates of Flavor Object

The binding mechanism in the somatomotor mouth area is proposed to comprise unimodal and multimodal representations of taste, smell, and oral somatosensation that arise when a stimulus is in the mouth. However, the current paucity of data on flavor processing necessitates a hypothetical rather than an empirical description of the proposed network, which is depicted in Figure 36.9

Certainly, odor object representations in the piriform cortex (Gottfried et al. 2006b; Wilson and Stevenson 2004) and OFC (Gottfried et al. 2006a; Schoenbaum and Eichenbaum 1995a,1995b) are likely to be key components of the flavor network. In addition, regions with overlapping representation of taste, odor, and oral somatosensation are likely to be critical. In humans, there is evidence from functional neuroimaging studies of overlapping responses to taste, smell, and oral somatosensation in the insula and overlying operculum (Cerf-Ducastel and Murphy 2001; de Araujo and Rolls 2004; Marciani et al. 2006; Poellinger et al. 2001; Savic et al. 2000; Small et al. 1999, 2003; Verhagen et al. 2004; Zald et al. 1998), and in the OFC (Francis et al. 1999; Frank et al. 2003; Gottfried et al. 2002a, 2002b, 2006a; Marciani et al. 2006; O’Doherty et al. 2000; Poellinger et al. 2001; Savic et al. 2000; Small et al. 1997, 1999, 2003; Sobel et al. 1998; Zald et al. 1998; Zald and Pardo 1997; Zatorre et al. 1992). In accordance with these findings in humans, single-cell recording studies in monkeys have identified both taste- and smell-responsive cells in the insula/operculum (Scott and Plata-Salaman 1999) and OFC (Rolls and Baylis 1994; Rolls et al. 1996).

Although not considered traditional chemosensory cortex, the anterior cingulate cortex receives direct projections from the insula and the OFC (Carmichael and Price 1996; Vogt and Pandya 1987), responds to taste and smell (de Araujo and Rolls 2004; de Araujo et al. 2003; Marciani et al. 2006; O’Doherty et al. 2000; Royet et al. 2003; Savic et al. 2000; Small et al. 2001, 2003; Zald et al. 1998; Zald and Pardo 1997), and shows supra-additive responses to congruent taste–odor pairs (Small et al. 2004). Therefore, it is possible that this region contributes to flavor processing. Moreover, a meta-analysis of all independent studies of taste and smell confirmed large clusters of overlapping activation in the insula/operculum, OFC, and anterior cingulate cortex (Verhagen and Engelen 2006).

There is also evidence for supra-additive responses to the perception of congruent but not incongruent taste–odor solutions in the anterodorsal insula/frontal operculum, anteroventral insula/ caudal OFC, frontal operculum, and anterior cingulate cortex (McCabe and Rolls 2007; Small et al. 2004). Such supra-additive responses are thought to be a hallmark of multisensory integration (Calvert 2001; Stein 1998). The fact that the supra-additive responses in these regions are experience-dependent strongly supports the possibility that these areas are key nodes of the distributed representation of the flavor object. In support of this possibility, an unpublished work suggests that there are differential responses to food versus nonfood odors, and that such responses occur in the insula, operculum, anterior cingulate cortex, and OFC (Small et al., in preparation).

Finally, neuroimaging studies with whole brain coverage frequently report responses in similar regions of the cerebellum (Cerf-Ducastel and Murphy 2001; Savic et al. 2002; Small et al. 2003; Sobel et al. 1998; Zatorre et al. 2000) and amygdala (Anderson et al. 2003; Gottfried et al. 2002a, 2002b, 2006b; Small et al. 2003, 2005; Verhagen and Engelen 2006; Winston et al. 2005; Zald et al. 1998; Zald and Pardo 1997) to taste and smell stimulation, although neither region shows supra-additive responses to taste and smell (Small et al. 2004). We have elected not to include these regions in the proposed network, but acknowledge that there is at least some empirical basis for further investigation of their role in flavor processing.

One important but still unresolved question regarding the neurophysiology of flavor perception is whether the process by which an odor object becomes part of a flavor percept results in changes to the odor object (Wilson and Stevenson 2004). Preliminary work suggests that the taste-like properties of food odors are encoded in the same region of insula that encodes sweet taste, and not in the piriform cortex or OFC (Veldhuizen et al. 2010). Subjects underwent fMRI scanning while being exposed to a weak sweet taste (sucrose), a strong sweet taste, two sweet food odors (strawberry and chocolate), and to sweet nonfood odors (rose and lilac). A region of insular cortex was identified that responded to taste and odor sweetness. This finding is consistent with a recent report that insular lesions disrupt taste and odor-induced taste perception (Stevenson et al. 2008). Moreover, it was found that the magnitude of insular response to food, but not nonfood odors, correlated with perceived sweetness. The selectivity of the association between response and sweetness perception strongly suggests that experience with an odor in the mouth as a food or flavor modifies neural activity, and that this occurs in the insula, but not in the piriform cortex. This, in turn, suggests that odor objects represented in the piriform cortex are not modified by flavor learning. In summary, it is proposed that bimodal taste–odor neurons in the OFC and anterior insula are changed during simultaneous perception of taste and retronasally sensed odor, whereas piriform neurons are not. Thus, we hypothesize that the flavor object comprises an unmodified odor object and modified bimodal cells that become associated within a distributed pattern of activation during initial binding.

Another critical question for understanding neural encoding of flavor objects is whether the entire active network is encoded or only a subset of key elements. For example, is activation of the somatomotor mouth area required to reexperience the flavor percept? If not, what are the key elements? The answers to these questions are currently unknown. However, as discussed above, it is possible that the taste signal is critical (Davidson et al. 1999; Synder et al. 2007).

36.6. ALTERNATIVE MODELS

Two other neural models for configural encoding of unitary flavor percepts have been proposed. First, Stevenson and Tomiczek (2007) consider the acquisition of taste-like properties in the context of synesthesia. They propose that a multimodal representation of flavors exists in a distributed network that includes the insula, amygdala, and OFC. This idea is similar to the proposed model. However, instead of emphasizing a binding mechanism related to referral, they conceive of taste–odor learning as an implicit synesthesia, with the odor as the inducer and the taste as the concurrent, or illusory, perception. The model hinges on the fact that odors have two pathways to the orbital cortex: a direct projection from the olfactory bulb and one reliant on a relay through the thalamus. It is argued that the thalamocortical pathway, which receives purely olfactory input, allows the multimodal representation activated by the direct pathway to be assigned as olfactory experience, giving rise to the perception that the odor has a taste. The second model was proposed by Verhagen and Engelen (2006), who, like us, highlight the importance of binding. However, they do not focus on oral referral and suggest a role for the hippocampus, or hippocampus-like mechanism, in binding and for the perirhinal cortex in the conscious perception of flavors (Verhagen 2007). Future research will determine which of these models—if any—is correct.

36.7. SUMMARY

We propose that during tasting, retronasal olfactory, gustatory, and somatosensory stimuli form a perceptual gestalt—the “flavor object”—the elements of which maintain their individual qualities to varying degrees. The development and experience of this percept is dependent on oral referral, for which neural processing in the somatomotor mouth area is deemed critical. An as-yet- unidentified neural mechanism within this region is hypothesized to bind the pattern of responses elicited by flavor stimuli. When the binding mechanism is active, unimodal inputs shape the selectivity of bimodal taste–odor neurons. Flavor objects are then encoded via configural learning as a distributed pattern of response across the somatomotor mouth area, multiple regions of insula and overlying operculum, orbitofrontal cortex, piriform cortex, and anterior cingulate cortex. It is these functionally associated regions that constitute the neural basis of the proposed flavor modality.

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