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Montmayeur JP, le Coutre J, editors. Fat Detection: Taste, Texture, and Post Ingestive Effects. Boca Raton (FL): CRC Press/Taylor & Francis; 2010.

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Fat Detection: Taste, Texture, and Post Ingestive Effects.

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Chapter 10Preference for High-Fat Food in Animals

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10.1. INTRODUCTION

The phenomenon of animals preferring high-fat foods has been accepted as natural behavior. Animals are equipped with fat not only for energy storage, but also for regulation of body temperature and as a source of many hormones. It is reasonable that animals eat and store fat based on physiological demands. On the other hand, eating an excessive amount of fat causes many metabolic diseases such as type II diabetes, atherosclerosis, and cardiovascular disease. Reflecting the current health situation in industrialized nations, fat studies are focused on why we overeat high-fat foods and how we can cope with accumulating body fat. Ironically, many tasty and palatable foods such as snack foods, ice cream, donuts, and so on, contain large amounts of fat. The high palatability of fatty foods has been reported in many articles. Animals, including humans, show a hedonic preference for fat that increases with fat concentration (Drewnowski and Greenwood, 1983; Imaizumi et al., 2000a). When it comes to dietary fat, we cannot regulate proper calorie intake, and so we consume more calories than we physiologically need. In a long-term drinking test for corn oil in mice, the mice continued to prefer corn oil and ingested excess calories beyond their physiological needs (Takeda et al., 2001a).

Why are fatty foods so tasty? Why do we lose our desire to balance calorie intake when ingesting fat? Researchers are increasingly interested in studying the palatable features of fat to address these simple questions. Accumulating data suggest that the high palatability of fat can be attributed to many factors, including its texture (Rolls et al., 2003; De Araujo and Rolls, 2004; Kadohisa et al., 2005), flavor (Ramirez, 1993; Kinney and Antill, 1996), taste (Gilbertson et al., 1997; Gilbertson, 1998; Abumrad, 2005; Laugerette et al., 2005; Matsumura et al., 2007), and postingestive effect (Sclafani and Vigorito, 1987; Suzuki et al., 2003).

In this chapter, we discuss a wide range of physiological responses to fat, from fat recognition on the tongue to laboratory animal behavior in response to fat.

10.2. POSSIBLE FACTORS INVOLVED IN THE HIGH PALATABILITY OF FAT

10.2.1. Taste

10.2.1.1. Receptors for Fatty Acids on the Tongue

Fatty foods are tasty and preferable. When mice were offered both fried potatoes and boiled potatoes at the same time, they significantly preferred fried potatoes (Imaizumi et al., 2001b). Mice also preferred a corn oil solution to vehicle during a 10 min two-bottle choice test paradigm (Takeda et al., 2000). How did mice recognize fat in the oral cavity in such a short period? In the past, researchers believed that the preference for dietary fat came mostly from its texture and flavor. However, the sensation of fat spreads throughout the oral cavity when we eat high-fat foods such as butter or fresh cream. Does fat have a recognizable taste? At the moment we do not have an appropriate word to describe the fatty taste, and we are still not sure that the fatty sensation in the oral cavity is one of taste. The authors of recent studies suggest that there may be fatty acid (FA) receptors on the tongue that play an important role in the recognition of FAs (Table 10.1).

TABLE 10.1

TABLE 10.1

Fatty Acids Receptors on the Tongue

CD36/FAT is an 88 kDa glycoprotein, originally discovered as an FA-binding protein (FABP) in adipocytes (Abumrad et al., 1993). Its role as a possible FAs recognition receptor on the tongue was first reported in rats (Fukuwatari et al., 1997). Northern blotting and immunohistochemical study showed the expression of CD36 in the circumvallate papillae, specifically localized in the apical parts of taste bud cells (Fukuwatari et al., 1997). In support of these data, CD36-null mice showed an attenuated preference for a linoleic acid solution. Furthermore, CD36-null mice with esophageal ligations displayed abolished pancreatic secretions in response to FAs (Laugerette et al., 2005). Finally, activation of c-fos in neurons of the nucleus of the solitary tract stimulated by FA deposition on the tongue of wild-type mice was abolished in CD36-null mice (Gaillard et al., 2007). Those data strongly suggest that CD36 on the tongue acts as an FA receptor.

In addition to CD36, the G protein–coupled receptor 120 (GPR120) was found in circumvallate, fungiform, and foliate papillae by real-time polymerase chain reaction (RT-PCR) and immunohistochemistry (Matsumura et al., 2007). GPR120 was first found in the colon as a long-chain FA recognition receptor (Hirasawa et al., 2005). GPR120 has a seven-transmembrane structure, which is different from the two-transmembrane structure of CD36 (Abumrad, 2005), but similar to the seven-transmembrane bitter, sweet, and umami receptors, which are also G protein–coupled receptors (Chandrashekar et al., 2006).

Polyunsaturated long-chain fatty acids (PUFAs), which are preferred by mice, are strong ligands for GPR120 (Hirasawa et al., 2005), suggesting that GPR120 on the tongue is also a possible fat recognition receptor. Recently, GPR40 was also found on the tongue in circumvallate, foliate, and a small number of fungiform papillae; therefore, it too, might be involved with the FA recognition on the tongue (Cartoni et al., 2007). Glossopharyngeal whole nerve recordings in GPR40 knockout (KO) mice showed a diminished response to oleic acid, linoleic acid, linolenic acid, and docosahexaenoic acid. Although GPR40 KO mice showed an attenuated preference for intake of corn oil, the mice’s electrophysiological as well as behavioral responses to FA solutions were normal, suggesting that other FA receptors besides GPR40 are important in the recognition of FAs. Considering these facts, there seem to be various kinds of FAs recognition receptors on the tongue that might have distinct roles.

TRPM5, a member of the transient receptor potential (TRP) family, has been reported as a possible downstream component of the FA receptors, signaling cascade. TRPM5 is a calcium-activated cation channel expressed in the taste receptor cells important for the detection of many tastants (Zhang et al., 2003; Damak et al., 2006). G protein–coupled taste receptors such as T1Rs, T2Rs, and mGluR4 signal through a common pathway involving the activation of phospholipase C (PLC), leading to the hydrolysis of phosphatidylinositol 4,5-biphosphate (PIP2) into inositol triphosphate (IP3) and diacylglycerol (DAG), which in turn stimulate the release of Ca2+. TRPM5 is coexpressed with the IP3 receptor and PLC beta 2, suggesting that TRPM5 is a part of the PLC-IP3 signaling pathway (Liman, 2007). TRPM5-null mice showed no licking response to a sweet tastant, a diminished preference ratio for sweet and umami tastants, and a reduced response to bitter taste (Damak et al., 2006). Sclafani et al. reported that TRPM5 KO mice showed no preference for soybean oil emulsion in the initial two-bottle choice test, while gustducin (one of the important signaling molecules in the taste cells) KO mice showed a normal response to the soybean oil (Sclafani, 2007). GPR40 and GPR120 were reported to be coexpressed with the TRPM5 (Cartoni et al., 2007). These findings suggest that TRPM5 but not gustducin is one of the signaling components that play a role in fat recognition on the tongue. Signaling pathways involved in fat recognition on the tongue are beginning to be uncovered, but much remains unknown and more research is needed to help us understand the oral perception of FAs.

10.2.1.2. How Do Rodents Recognize Fat in the Oral Cavity?

Dietary oil consists of >90% triacylglycerols, and a small percentage of mono- or diacylglycerols and FAs. This fact raises the question of whether we recognize triacylglycerol, monoacylglycerol, diacylglycerol, or FAs when we perceive the taste of fat. So far no receptor for triacylglycerols has been identified, whereas several FA receptors, such as CD36 (Abumrad et al., 1993), FABP (Stremmel et al., 1985), fatty acid transporters (FATPs), GPR40 (Briscoe et al., 2003), and GPR120 (Hirasawa et al., 2005) have been found expressed in various organs. As described above, CD36, GPR40, and GPR120 are expressed in the circumvallate papilla. In behavioral studies, rats prefered 1% oleic acid, linoleic acid, and linolenic acid to 0.3% xanthan gum (Tsuruta et al., 1999). A similar preference for FAs is also observed in mice (Yoneda et al., 2007a), suggesting that rodents can recognize FAs on the tongue. Interestingly, rats also display a preference for pure triacylglycerol (Kawai and Fushiki, 2003). When offered a choice between a triolein solution and a vehicle, rats showed a significant preference for the triolein solution. How do rodents recognize triolein on the tongue? Kawai et al. answered this simple question by showing that when rats were offered a triolein solution with the lipase inhibitor orlistat, their preference for triolein was abolished. Therefore, lingual lipase released from Ebner’s glands cleaves triacylglycerols on the tongue to release free FAs (Kawai and Fushiki, 2003) (Figure 10.1). The small percentage of free FAs found in dietary oil or those released from triacylglycerols are recognized on the tongue, possibly through an FA receptor such as CD36 or GPR120, which might be important to evoke the fat sensation in the oral cavity of rodents. However, it seems difficult to extrapolate the results from the animal experiments to a model for humans, since humans have a lower level of lingual lipase than rodents. Humans have an orosensory mechanism to detect FAs and perceive them as attractive ingredients. Free FAs released voluntarily from triacylglycerols in foods might be important for humans as a signal of fat.

FIGURE 10.1. Schematic representing the mechanisms of fat recognition on the tongue.

FIGURE 10.1

Schematic representing the mechanisms of fat recognition on the tongue. Dietary fats consist of mostly triacylglycerols. Triacylglycerols (triolein in this figure) are digested by the lingual lipase secreted from Ebner’s glands. In a few seconds, (more...)

The fact that rodents recognize FAs on the tongue has also been supported by patch clamp experiments. In isolated rat taste receptor cells, extracellular application of FAs inhibited the delayed rectifying K+ channel (Gilbertson et al., 1997, 1998). This effect was limited to polyunsaturated fats with double bonds in the cis configuration (linoleic acid C18:2, linolenic acid C18:3, arachidonic acid C20:4, eicosapentaenoic acid C20:5, docosahexaenoic acid C22:6), suggesting that fat was recognized in the oral cavity and inhibition of the delayed rectifying K+ channel is involved in the signal transduction mechanism for FAs (Gilbertson et al., 1997). As described above, TRPM5 is expressed in taste receptor cells and may be one of the downstream signaling mechanisms of GPCRs in the taste cells.

10.2.1.3. Oral Stimulation by FA Evokes a Physiological Response

Sensory stimulation induces many metabolic responses within a few minutes. This nerve-mediated phenomenon is known as the cephalic phase response. An example is provided by the induction of pancreatic enzyme secretion after stimulation of the tongue by dietary oils or FAs. In esophagotomized rats, oral stimulation by corn oil or long-chain fatty acids (oleic acid, linoleic acid, linolenic acid) increased pancreatic enzyme secretion, but stimulation with the middle-chain fatty acid, caprylic acid, or the FA derivative, methyl linoleate did not have this effect (Hiraoka et al., 2003). These data imply that the carboxylated groups and the length of the FA chain are also important in the recognition of FAs on the tongue. In support of these data, CD36-null mice were reported to be devoid of cephalic phase response when linoleic acid was applied to the tongue (Laugerette et al., 2005), which suggests that some long-chain FAs with double bonds are potentially recognized through the CD36 receptor on the tongue, thereby sending a signal to the brain that leads to the initiation of the cephalic phase response.

10.2.2. Odor

The odor of food is an important signal that tells us whether we can eat and swallow certain foods. Fatty foods have a distinct odor. While the flavors in fatty foods/dietary oils come mostly from the free FAs or flavor components from various ingredients, the responsible signal in dietary oils is not yet well understood. Since many studies about odor in dietary oils have been devoted to the negative effect of oil flavor due to oxidation, polymerization, hydrolyzation, and so on, our understanding of the stimulation of appetite by the odor in dietary oil is limited at present. Within the limited reports of studies related to the FAs in dietary oil, short- to middle-chain FAs were recognized in a special area of the olfactory bulb (Mori et al., 1992), while long-chain FAs were considered to be odorless.

Deep-fried foods have a distinctive and attractive odor. Seven volatile compounds (2,4-decadienal, 2-heptenal, 2-octenal, 2,4-decadienal, 2,4-octadienal, 2,4-nonadienal, and (E,Z)2,4-nonadienal) were found to produce the deep-fried odor in trilinolein (Warner et al., 2001). Also, 2-alcans (aldehydes) were detected during the heating of triolein, which may contribute to its distinctive odor. This indicates that the odor in fatty foods might come in part from by-products formed during cooking.

How important is odor when selecting dietary fat? Olfactory-blocked mice either treated with ZnSO4 to destroy olfactory sensory neurons or for which the olfactory nerve was cut were used to study whether oil flavor is the primary factor leading to the selection of fatty foods. In mice with a sectioned olfactory nerve, no preference for high-fat foods was observed (lab chow to which was added 9% vegetable oil), while sham operated or normal mice showed a preference for high-fat foods (Kinney and Antill, 1996), thus highlighting the importance of the olfaction system when selecting dietary oil. On the other hand, Ramirez reported that rats with anosmia induced by an olfactory bulbectomy showed reduced but not abolished preference for 1% corn oil (Ramirez, 1993). To support these data, Takeda et al. reported that ZnSO4- treated mice showed a preference for corn oil at concentrations greater than 5% but could not discriminate between the vehicle and a 1% solution of corn oil (Takeda et al., 2001b), suggesting that, at low concentration, corn oil is chosen based on olfactory cues.

Thus, odor cues play a role in oil detection at low concentrations; however, olfactory-blocked rodents can still detect oil at higher concentrations.

10.2.3. Texture

Another specific feature of oil is its oily texture, which was thought to come mainly from its viscosity. However, Ramirez showed that rats conditioned to avoid the oil viscosity (67 cp) by injection of LiCl avoided oils (triolein, mineral oil, silicon oil) with a wide range of viscosities (5–203 cp), but did not avoid an oil-free solution of similar viscosity (Ramirez, 1994). Similarly, there was no direct relation between the perceived fat content and viscosity in sensory assessments by humans (Mela et al., 1994), suggesting that viscosity is not a main component of fat perception.

How much does the oily texture contribute to fat preference? Some neurons in the amygdala responded not only to fat, but also to nonfat oils such as silicone oil and mineral oil (Kadohisa et al., 2005). Interestingly, those neurons did not respond to FAs and lauric acid, suggesting that some neurons in the amygdala are tuned to the texture itself independently of FA recognition, a modality important in recognizing fat-like foods in the mouth (Kadohisa et al., 2005). In another experiment, a one-bottle test in nondeprived rats showed that 30% corn oil and 30% mineral oil were equally acceptable. However, when rats are fasted, the preference for corn oil emulsion is increased in two-bottle tests, suggesting that emulsified oil is attractive to the rat, but the postingestive effects of corn oil likely enhanced the preference for corn oil (Ackroff et al., 1990). In summary, these results indicate that oily texture is one of the important signals for oily foods recognition but it is not the main factor guiding fatty foods selection.

10.2.4. Postingestive Effect of Dietary Oil

A specific feature of dietary oil is that it is high in calories. Triacylglycerol has 9 kcal/g, which is more than two times greater than the amount of calories in carbohydrates (4 kcal/g) and proteins (4 kcal/g). The high calorie count in fat might contribute to the palatability of fatty foods. When rats are offered a high-fat (HF) diet their food intake and preference for oil are increased compared with rats fed a high-carbohydrate diet (Reed et al., 1990; Lucas et al., 1998). Rats fed the HF diet with sham feeding increased their intake on the first try but not on a subsequent try, suggesting that sensory stimulation is important on the first try, before postingestive effects are in place. This also points out the important role of the postingestive effect in the high palatability of fat (Reed et al., 1990). Experiments regarding the postingestive effect of dietary oil are discussed further in the next section.

10.3. BEHAVIORS DRIVEN BY THE HIGH PALATABILITY OF DIETARY FAT AND FATTY ACIDS

10.3.1. Behavioral Assays for the Measurement of Food Palatability

There are various methods for assaying the high palatability of foods (Table 10.2). The two-bottle choice test (Figure 10.2a) is a conventional method for determining preference. In this test, rodents are offered a pair of bottles simultaneously, and the consumed volume is measured for a defined time. If the test period is short (under 10 min), the preference is considered to be an indication of orosensory stimulation. If the test period is longer (>30 min), the preference is thought to reflect orosensory stimulation as well as postingestive effects. The two-bottle choice test is simple and easy to perform, but it allows one to assess only the relative preference between the two bottles.

TABLE 10.2

TABLE 10.2

Available Behavioral Assays to Test Fat Preference

FIGURE 10.2. Behavioral assays available to assess food palatability.

FIGURE 10.2

Behavioral assays available to assess food palatability. (a) The two-bottle choice test is used to understand which solution is preferable between two samples. The preference value (one-bottle intake divided by the total intake) or intake volume for a (more...)

Another way to assess the preference for food is the licking test (Figure 10.2b), which was applied based on the phenomenon that animals show a high initial licking rate for a palatable solution. The intensity of food palatability was shown as an absolute value (the initial licking rate). The procedure, an animal is placed in the test chamber and allowed access to a stainless steel drinking spout from which the test solution is offered. The licking rate is recorded by a computer. In this procedure, the postingestive effects are completely excluded, since the initial licking rate is usually measured within a minute (30–60 s). Therefore, the initial licking rate is considered to reflect the preference to the solution in the oral sensation. For a detailed description of the licking test, refer to Yoneda et al. (2007a).

When we eat fatty foods, we find them tasty partly because of sensory stimulation, which, along with postingestive effects, makes us eager to eat more. The conditioned place preference (CPP) test (Figure 10.2c) and the operant task (Figure 10.2d) have also been used recently to measure the intense palatability of food, including oral stimulation and the postingestive effect of a test sample. Both methods were developed to study the reinforcing or rewarding effect of addictive drugs such as morphine and opioids, and therefore measure more than just the palatability of foods.

The CPP test measures reinforcing effects based on the preferences for a specific environment associated with a preferable stimulus. A detailed description of the CPP test for foods is given in Guyon et al. (1993) and Imaizumi et al. (2000b). In short, the CPP test chamber consists of two boxes, a box with lighting (light box) and a box without lighting (dark box). The boxes are connected through a guillotine door in the middle. The CPP test runs over 10 days. From day 1 to day 3, mice are acclimated to the boxes and baseline behaviors in both boxes are measured. Time spent on day 3 in the light box is used as the baseline preference. Day 4 to day 9 is used as a conditioning period, during time the which mice are alternately conditioned for a food test sample in the light box or for water in the dark box. Day 10 is the test day. Mice are freely moved to both boxes without any food samples, and the time spent in the light box is measured. The CPP index is used as the difference between the time spent on day 3 (baseline) and that on day 10 (test day). If the time spent on day 10 is significantly increased, it is assumed that the test sample elicited a rewarding effect.

The operant task is another well-known method for studying drug addiction; that can also be used to assess the reinforcing effects of foods (Elmer et al., 2002; Hayward et al., 2002; Ward and Dykstra, 2005). Progressive ratio (PR) schedules in the operant task provide the reinforcing properties of gustatory stimuli as the absolute value for each tastant (Reilly, 1999). The break point in the PR test, which is defined as the last number of lever presses to get the reinforcer, is taken as an index of the reinforcer value. Using this method, sucrose was shown to be a positive reinforcer in rats (Reilly, 1999). Both the CPP test and the operant task are important tools for evaluating the rewarding effects of foods.

10.3.2. Rodent Preferences Point Out the High Palatability of Dietary Fat

All assays point to a preference for dietary oil by rodents (Figure 10.3). Ten-minute two-bottle choice tests show that mice prefer corn, canola, or mixed vegetable oil over vehicle (Figure 10.3a) (Takeda et al., 2000). In a test of various concentrations of corn oil, mice consistently preferred the higher concentration of corn oil to the lower concentration (Yoneda et al., 2007a) with 100% corn oil being the most preferable solution, suggesting that mice can discriminate oil concentration in the oral cavity. The postingestive effect cannot be ignored during this test since 10 min is enough time for the oil to reach the digestive organs. To evaluate oral stimulation caused by dietary oil, the licking test is useful as it evaluates the reaction to a sample solution within 60 s. In accordance with the two-bottle choice test results, the initial licking rate for corn oil was significantly higher than for the vehicle (Figure 10.3b), and the licking count increased in a concentration-dependent manner (Yoneda et al., 2007a). In addition to dietary oil, mice prefer low concentrations of FAs solutions. Solutions of 0.25%–1% linoleic acid (LA), which is a main FA in corn oil, are preferred over the vehicle in a two-bottle choice test, while solutions at concentrations greater than 1% are not preferred by mice (Yoneda et al., 2007a). Considering the finding that the lingual lipase digested the triacylglycerol (Kawai and Fushiki, 2003) and released small amounts of FA on the tongue, it is reasonable to conclude that mice prefer low concentrations of FA. The fact that the mice preferred not only dietary oil but also a low concentration of FA solution during both a two-bottle choice test and a licking test suggests that FAs in fatty foods have a key role in the detection of fat in the oral cavity.

FIGURE 10.3. The preference or rewarding effect for corn oil as evaluated by several behavioral assays.

FIGURE 10.3

The preference or rewarding effect for corn oil as evaluated by several behavioral assays. (a) Two-bottle choice test between vehicle (mineral oil) and 100% corn oil. Mice were given a choice between a bottle of pure mineral oil and one of pure corn oil, (more...)

10.3.3. Postingestive Effect and Rewarding Effect of Dietary Fat

The postingestive effect has long been considered an important factor in food selection and preference. During an experiment in which rats were given a choice between a sucrose octaacetate (SOA)-polycose solution and pure sucrose powder, they initially preferred the sucrose powder, but during the latter part of the test session (5–8 days), the rats developed a preference for the SOA-polycose solution over the sucrose powder, suggesting that a carbohydrate-mediated postingestive effect affected their preference (Sclafani, 1987). In the CPP test, rats showed a place preference for 18% sucrose but not for 0.1% saccharin, a sweetener with no calories, although the licking response for the saccharin solution was similar to that for the sucrose (Agmo and Marroquin, 1997). Interestingly, the rats showed a place preference when a glucose injection was combined with saccharin drinking. These results suggest that a postingestive effect contributes to the food selection behavior. This phenomenon was also applied to fat preference and its associated behavior. The rodent appetite for fat seems to be stronger than that for carbohydrate.

When mice were offered fried potatoes and boiled potatoes at the same time, they significantly preferred the fried potatoes, whether the oil used for frying had been lard or corn oil (Imaizumi et al., 2001a,b). When fed isocaloric diets of high-fat (HF) or high-carbohydrate content, rats consumed more of the HF diet, suggesting that there is a postingestive action of the HF diet-stimulating food intake (Lucas et al., 1998). Taken together, these data suggest that the postingestive effect of dietary fat also contributes to increased fat intake.

When given a mixture of glucose, saccharin, and corn oil solution, rats have trouble regulating calorie intake while this ability is not affected when given only water and food or glucose solution (Takeda et al., 2001a).

Thus, dietary fat ingestion seems to have an impact on the regulation of energy intake in rats. This phenomenon might be explained by the rewarding and reinforcing effects of dietary oil as revealed by CPP tests for corn oil (Figure 10.3c) (Imaizumi et al., 2000b). Time spent in the light box after being conditioned for corn oil increased significantly, suggesting that corn oil stimuli elicited a rewarding effect. A reinforcing effect following stimulation by corn oil was also observed in the operant task (Figure 10.3d) (Ward et al., 2007; Yoneda et al., 2007b), where the break point for the corn oil was significantly increased, thus pointing to a reinforcing effect. Furthermore, this reinforcing effect of corn oil was increased in a concentration-dependent manner since the reinforcing effects of 50% and 100% corn oil were significantly higher compared with that of 0% corn oil (Yoneda et al., 2007b).

These results show that the high palatability of dietary fat derives not only from its orosensory recognition but also from postingestive factors. The rewarding or reinforcing effect of dietary fat might be one reason why animals lose the ability to appropriately regulate calorie intake and proceed to overeat fatty foods.

10.3.4. Fat Substitutes and the Postingestive Effect

Compared to proteins and carbohydrates, FAs are high in calories (9 kcal/g), which might be one reason, together with high intake, for the increased incidence of obesity worldwide. To help people avoid overeating fatty foods, researchers have developed fat substitutes with a similar texture but fewer calories in the hope that they might be helpful.

A wide variety of fat substitutes have been developed to reduce fat intake from dietary foods (Wylie-Rosett, 2002). Most of these fat substitutes, which were derived from a carbohydrate or protein base, were designed to mimic the texture of fat. In addition, a few fat-based fat substitutes have been used, including sugar–fatty acid esters or mono- or diacylglycerol instead of triacylglycerol.

In the United States, Olestra™, which consists of FAs esterified to sucrose, was permitted for use in the preparation of snacks. In a 2-week trial with human subjects using Olestra, subjects had 8% lower total energy intake and 11% lower fat intake when using Olestra compared with subjects not using it (Hill et al., 1998). In a 1-year study of heavy use of Olestra, energy intake from fat decreased 2.7%, although the total energy intake was not different from that in those who did not use Olestra (Patterson et al., 2000). Therefore, a low calorie fat substitute can be used as an alternative source of fat; however, the low calorie count does not help to reduce total energy intake, thus highlighting the large contribution of the postingestive effect in fat consumption. In a supportive study investigating the effect of the postingestive phenomenon on food intake, subjects were preloaded with yogurt adulterated with either saccharin, glucose, or starch. The results show that during the following meal, intake was increased in the saccharin-preloaded group, suggesting that noncalorie sweeteners do not have a reducing effect on total calorie intake (Rogers and Blundell, 1989). Therefore, people trying to lose weight by using fat or sugar substitutes should be careful in monitoring their total calorie intake.

To understand the postingestive effect of fat, we used one of the fat substitutes, sorbitol FA ester (SOR), in an animal study. SOR consists of FAs esterified onto a sorbitol molecule, which is nondigestible and contains few calories (1.5 kcal/g). When mice were offered both 2% sorbitol FA esters and its vehicle at the same time in a two-bottle choice test for 10 min, the mice significantly preferred SOR. In a long-term two-bottle choice test between 100% corn oil and 100% SOR, mice drank equal amounts of the two solutions during the first 30 min. However, the mice showed a preference for corn oil after 30 min and up to 24 h, suggesting that mice considered that SOR was similar to corn oil for the first 30 min but not thereafter. In terms of texture in SOR, mice with a conditioned taste aversion to corn oil avoided SOR, and vice versa, suggesting that oral cues did not allow them to discriminate between the two solutions. Therefore, the preference of corn oil over SOR observed after 30 min might be related to the postingestive effect of corn oil.

In another series of experiments, mice were intragastrically administered corn oil before CPP for SOR. Interestingly, SOR paired with calories elicited a rewarding effect. Neither an intragastric injection of corn oil alone nor oral stimulation of SOR alone elicited the rewarding effect, suggesting that both oral stimulation and caloric content are important in eliciting the rewarding effect in the CPP test (Suzuki et al., 2003). To understand the mechanism of the reinforcing effect of dietary oil, a beta-oxidation blocker (mercaptoacetate: MA) was used since beta-oxidation is a pathway toward using FAs as an energy source. Intraperitoneal injection of MA before conditioning for corn oil in the CPP test attenuated the reinforcing effect of corn oil, while it did not affect the reinforcing effect of sucrose (Figure 10.4) (Suzuki et al., 2006), suggesting that the process of beta-oxidation after ingesting the corn oil is important for supplying energy information. In terms of the high palatability of dietary oil, not only the sensory stimulus, but also the postingestive effect seem to be important.

FIGURE 10.4. Postingestive effects are important for the rewarding effect in the CPP test.

FIGURE 10.4

Postingestive effects are important for the rewarding effect in the CPP test. Mice were conditioned for the test sample in the light box and for water in the dark box. Thirty minutes before beginning the conditioning trials, mice were injected with a (more...)

If the postingestive effect of corn oil is important for its rewarding effect, then one can ask whether oil-like oral stimulation needs to be paired with energy from fat through the postingestive effect or energy from carbohydrates or proteins to elicit the same rewarding effect. To address this question, we used a CPP test with glucose calorie loading in the stomach for SOR. Mice were intragastrically injected with glucose into the stomach and experienced oral stimulation with the oil-like texture of SOR. Interestingly, even though glucose as a source of calories was intragastrically injected before conditioning for SOR, the rewarding effect was elicited (Suzuki et al., 2006). These results suggest that an energy-sensing mechanism is important in eliciting the rewarding effect. At the moment, it remains unclear which energy-sensing mechanism is involved in the rewarding effect of corn oil.

These studies imply that using a fat substitute might be helpful in reducing calorie intake from fat but not in decreasing total calorie intake. To overcome the high palatability of fatty foods, we should consider not only the sensory similarities of these substitutes but also the contribution of postingestive effects on their palatability.

10.4. REWARDING EFFECT OF DIETARY FAT: CENTRAL MECHANISMS

10.4.1. Possible Link between Taste and Peripheral Information

How are taste information and peripheral information linked? Interestingly, taste cells from the tongue and enteroendocrine cells from the gut are paraneurons (Fujita, 1991), which share common signaling mechanisms. These cells receive chemical stimuli on the apical side and then transmit the information by releasing neurotransmitters on their basolateral side. Studies of the response to the same stimulus elicited by taste cells and enteroendocrine cells support the evidence that they share signaling mechanisms and cooperate to elicit an appropriate behavioral response. Taste markers such as alpha-gustducin, T2Rs, and T1R3 are expressed in the gastrointestinal tract (Rozengurt, 2006; Margolskee et al., 2007; Sclafani, 2007), and it was reported recently that the T1R3 + T1R2 receptor complex serves as a sugar sensor in the gut. Detection of sugar in the lumen of the intestine regulates glucose transporter and is followed by the secretion of hormones such as GLP-1 and GIP, suggesting that taste receptors in the intestine play an important role in glucose homeostasis (Margolskee et al., 2007). Interestingly, CD36 and GPR120, two FA receptors expressed in the tongue, were first found in the intestine (Chen et al., 2001; Hirasawa et al., 2005). It is possible that food selection and preference come from a complex combination of tongue detection and gut detection.

10.4.2. Brain Mechanism Underlying the Rewarding Effect

The brain mechanisms involved in dietary fat overconsumption have been studied. It is well known that the reinforcing effects of many addictive drugs are mediated via the dopaminergic system. Recent data suggest that food reward is also under the control of the dopaminergic system in the brain; more precisely, D1 and D2 dopamine receptors are candidate receptors for this effect. Which receptor type is involved in the rewarding effect or the reinforcing effect of dietary oil? Pretreatment with D1 antagonists, SCH23390 (0.03 mg/kg) and haloperidol (0.1 mg/kg), antagonized the rewarding effect in the CPP test. On the other hand, (±)-sulpiride, a D2 antagonist, did not affect reward in the CPP test, suggesting that the rewarding effect elicited by the dietary oil might be mediated via D1 receptors in the brain (Imaizumi et al., 2000b). However, the break point for corn oil was attenuated by pretreatment with (−)-sulpiride, a D2 receptor antagonist, in the operant PR test, while SCH23390, a D1 receptor antagonist, did not influence the break point (Yoneda et al., 2007b). It seems that the reinforcing effect of corn oil in the operant task is mediated through D2 receptors in the operant task. This discrepancy between the CPP test and the operant test comes from the detecting system in the test. Recent studies suggest that D1 receptors in particular contribute to the instrumental and the reward-related incentive learning process (Kelley et al., 1997; Dalley et al., 2005). D1 antagonists might affect the learning process in the CPP test, since subjects were pretreated with those drugs before they were conditioned for corn oil.

Using microdialysis methods in rats implanted with gastric fistulae, Liang et al. reported that oral stimulation by corn oil released dopamine in the nucleus accumbens (Liang et al., 2006). This result also implies that taste stimulation by corn oil directly affects certain brain mechanisms.

The opioidergic system is related to food reinforcement (Solinas and Goldberg, 2005; Smith and Berridge, 2007) and is involved in the reinforcing effect of corn oil. Naloxone, an opioid receptor antagonist, was reported to reduce the preference for high-fat foods in human subjects. In other studies, opioid agonists influenced the intake of high-fat diets (Ookuma et al., 1998; Zhang et al., 1998). In the CPP test, a corn oil–induced CPP was diminished by treatment with naloxone, the μ opioid receptor antagonist 7-benzylidenenaltrexone (BNTX), or the δ opioid receptor antagonist naltriben. U-50488H, an opioid agonist of the κ receptor, which was reported to exert the opposite actions of μ receptor, also blocked corn oil–induced CPP, although it increased the corn oil intake in mice (Imaizumi et al., 2001b). These data imply that not only the dopaminergic system but also the opioidergic system could be involved in the reinforcing effect of fat.

How and when are opioids and dopamine released and put to action in the brain for the intake of dietary oil? Mizushige et al. reported that the mRNA level of pro-opiomeranocortin (POMC), a beta-endorphin precursor, in the hypothalamus was increased in rats given corn oil for five consecutive days. Interestingly, the increase of POMC mRNA was observed just before the ingestion of corn oil, while after corn oil ingestion, it was decreased (Figure 10.5). If the rats were kept away from corn oil on the test day, a high level of POMC mRNA was maintained for more than 30 min (Mizushige et al., 2006). These results suggest that the beta-endorphin system is related to the anticipation of corn oil intake. In accordance with these results, daily corn oil ingestion paired with a daily treatment of naloxone for 5 consecutive days did not lead to an increased preference for corn oil in the licking test (Figure 10.6), suggesting that the strong palatability of corn oil was supported by the opioidergic system. Those results also support our conclusion that brain mechanisms taking place after the ingestion of corn oil are important for inducing an appetite for corn oil.

FIGURE 10.5. Rats were provided with either a vehicle (0.

FIGURE 10.5

Rats were provided with either a vehicle (0.3% xanthan gum solution) or 5% corn oil at the same time each day for five consecutive days. On test day (day 6), the hypothalamus was removed 60 min before presentation, 0 (just before presentation), 30, or (more...)

FIGURE 10.6. Effect of an opioid receptor antagonist on the preference for corn oil.

FIGURE 10.6

Effect of an opioid receptor antagonist on the preference for corn oil. (a) Animals were provided with 5% corn oil or a vehicle (mineral oil) for 5 days. Licking rates for 5% corn oil were gradually increased over 5 days, but not those for the vehicle. (more...)

It remains unclear whether the dopaminergic system also plays a role in the appetite for corn oil. It is possible that both the opioid and dopaminergic systems cooperate to elicit a strong appetite for oil.

10.5. CONCLUSION

Rodents prefer fatty foods. Taste, smell, and texture are all important orosensory factors behind the high palatability of dietary fats. Of particular interest are FAs released from triglycerides by the lingual lipase on the tongue and possibly recognized by a receptor in the circumvallate papillae (Gpr120, CD36). Via these receptors, signals are transmitted to the brain through the taste nerves innervating the taste buds. Subsequently, ingested oil is not only digested and absorbed in the gastrointestinal tract, but also sends signals to the brain through an unknown mechanism. The information from orosensory receptors and peripheral tissue is integrated in the brain, resulting in a strong appetite for fatty foods (Figure 10.7). Understanding the mechanism of fat recognition will help us develop a strategy for coping with the high palatability of attractive foods, which will be conducive towards the prevention of overeating.

FIGURE 10.7. Schematic overview of the mechanisms underlying the high palatability of dietary fats.

FIGURE 10.7

Schematic overview of the mechanisms underlying the high palatability of dietary fats. When animals eat dietary fats, sensory signals such as taste, smell, and texture are transmitted to the brain. The taste signal from the tongue is especially important (more...)

ACKNOWLEDGMENT

Most of our work in this chapter was supported by the Program for the Promotion of Basic Research Activities for Innovation Bioscience.

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