Food sensory characteristics: their unconsidered roles in the feeding behaviour of domestic ruminants

When domestic ruminants are faced with food diversity, they can use pre-ingestive information (i.e. food sensory characteristics perceived by the animal before swallowing the food) and post-ingestive information (i.e. digestive and metabolic consequences, experienced by the animal after swallowing the food) to evaluate the food and make decisions to select a suitable diet. The concept of palatability is essential to understand how pre- and post-ingestive information are interrelated. It refers to the hedonic value of the food without any immediate effect of post-ingestive consequences and environmental factors, but with the influence of individual characteristics, such as animal's genetic background, internal state and previous experiences. In the literature, the post-ingestive consequences are commonly considered as the main force that influences feeding behaviour whereas food sensory characteristics are only used as discriminatory agents. This discriminatory role is indeed important for animals to be aware of their feeding environment, and ruminants are able to use their different senses either singly or in combination to discriminate between different foods. However, numerous studies on ruminants’ feeding behaviour demonstrate that the role of food sensory characteristics has been underestimated or simplified; they could play at least two other roles. First, some sensory characteristics also possess a hedonic value which influences ruminants’ intake, preferences and food learning independently of any immediate post-ingestive consequences. Further, diversity of food sensory characteristics has a hedonic value, as animals prefer an absence of monotony in food sensory characteristics at similar post-ingestive consequences. Second, some of these food sensory characteristics become an indicator of post-ingestive consequences after their initial hedonic value has acquired a positive or a negative value via previous individual food learning or evolutionary processes. These food sensory characteristics thus represent cues that could help ruminants to anticipate the post-ingestive consequences of a food and to improve their learning efficiency, especially in complex environments. This review then suggests that food sensory characteristics could be of importance to provide pleasure to animals, to increase palatability of a food and to help them learn in complex feeding situations which could improve animal welfare and productivity.     

LEARNED FLAVOR CUES INFLUENCE FOOD INTAKE IN HUMANS

These studies examined the influence of learned flavor cues on daily food intake in 28, normal-weight adults. Subjects were trained to associate distinctly flavored high or low calorie lunches with their postingestive effects. Following training, the flavors in the lunches were switched. Twenty-five percent of subjects (responders) adjusted their daily food intake based on their acquired sensory experience and were initially misled by the changes in the flavor cues; i.e., following the flavor switch, responders consumed additional or fewer calories based on the expected rather than actual energy intake of the meals. Energy intake gradually returned to baseline levels. The remaining subjects (nonresponders) were not misled by the flavor switch and maintained their customary level of intake. Responses were more pronounced following conditioning with the high calorie as compared to the low-calorie lunch. These data suggest that sensory cues may play an important role in the control of long-term food intake in individuals who are sensitive to such training.     

Food reward in the absence of taste receptor signaling

Food palatability and hedonic value play central roles in nutrient intake. However, postingestive effects can influence food preferences independently of palatability, although the neurobiological bases of such mechanisms remain poorly understood. Of central interest is whether the same brain reward circuitry that is responsive to palatable rewards also encodes metabolic value independently of taste signaling. Here we show that trpm5-/- mice, which lack the cellular machinery required for sweet taste transduction, can develop a robust preference for sucrose solutions based solely on caloric content. Sucrose intake induced dopamine release in the ventral striatum of these sweet-blind mice, a pattern usually associated with receipt of palatable rewards. Furthermore, single neurons in this same ventral striatal region showed increased sensitivity to caloric intake even in the absence of gustatory inputs. Our findings suggest that calorie-rich nutrients can directly influence brain reward circuits that control food intake independently of palatability or functional taste transduction.     

mu-Opioid receptor stimulation in the nucleus accumbens elevates fatty tastant intake by increasing palatability and suppressing satiety signals

Infusion of a μ-opioid receptor (MOR) agonist into the nucleus accumbens (NAcc) drives voracious food intake, an effect hypothesized to occur through increased tastant palatability. While intake of many palatable foods is elevated by MOR stimulation, this manipulation has a preferential effect on fatty food ingestion. Consumption of high-fat foods is increased by NAcc MOR stimulation even in rats that prefer a carbohydrate-rich alternative under baseline conditions. This suggests that NAcc MOR stimulation may not simply potentiate palatability signals and raises the possibility that mechanisms mediating fat intake may be distinct from those underlying intake of other tastants. The present study was conducted to investigate the physiological mechanisms underlying the effects of NAcc MOR stimulation on fatty food intake. In experiment 1, we analyzed lick microstructure in rats ingesting Intralipid to identify the changes underlying feeding induced by infusion of a MOR-specific agonist into the NAcc. MOR stimulation in the NAcc core, but not shell, increased burst duration and first-minute licks, while simultaneously increasing the rate and duration of Intralipid ingestion. These results suggest that MOR activation in the core increases Intralipid palatability and attenuates inhibitory postingestive feedback. In experiment 2, we measured the effects of MOR stimulation in the NAcc core on consumption of nonnutritive olestra. A MOR-specific agonist dose dependently increased olestra intake, demonstrating that caloric signaling is not required for hyperphagia induced by NAcc MOR stimulation. Feeding induced by drug infusion in both experiments 1 and 2 was blocked by a MOR antagonist. In experiment 3, we determined whether MOR activation in the NAcc core could attenuate satiety-related signaling caused by infusion of the melanocortin agonist MTII into the third ventricle. Suppression of intake caused by MTII was reversed by MOR stimulation. Together, our results suggest that MOR stimulation in the NAcc core elevates fatty food intake through palatability mechanisms dependent on orosensory cues and suppression of satiety signals inhibiting food intake.     

Food preferences and aversions in human health and nutrition: how can pigs help the biomedical research?

The establishment of food preferences and aversions determines the modulation of eating behaviour and the optimization of food intake. These phenomena rely on the learning and memory abilities of the organism and depend on different psychobiological mechanisms such as associative conditionings and sociocultural influences. After summarizing the various behavioural and environmental determinants of the establishment of food preferences and aversions, this paper describes several issues encountered in human nutrition when preferences and aversions become detrimental to health: development of eating disorders and obesity, aversions and anorexia in chemotherapy-treated or elderly patients and poor palatability of medical substances and drugs. Most of the relevant biomedical research has been performed in rodent models, although this approach has severe limitations, especially in the nutritional field. Consequently, the final aim of this paper is to discuss the use of the pig model to investigate the behavioural and neurophysiological mechanisms underlying the establishment of food preferences and aversions by reviewing the literature supporting analogies at multiple levels (general physiology and anatomy, sensory sensitivity, digestive function, cognitive abilities, brain features) between pigs and humans.     

Evaluation of effects (symptoms and palatability) after ingestion of "Gran Soleil" in healthy volunteers

A good digestion is essential to maintain a healthy status. It is known that physiological digestive processes could be improved by the ingestion of some medicinal plants, while specific foods can facilitate the occurrence of gastrointestinal symptoms. Moreover, sensory properties of food seem to also influence digestion. We assessed the influence on physiological digestive processes of two Gran Soleil (GS) products containing a mixture of digestive plant extracts, citrus juices and liquors. We evaluated, in 10 healthy volunteers, the eventual occurrence of gastrointestinal symptoms after their ingestion and measured their palatability. Ingestion of GS did not cause significant gastrointestinal symptoms. Moreover, the palatability median score shows a good appreciation of the products. In conclusion, it is possible to suppose that a product with a good palatability, able to support and maintain a good digestive condition, derives from the mixture of digestive herbs, citrus juices, liquor and other ingredients.     

Modulation of sweet responses of taste receptor cells

Taste receptor cells play a major role in detection of chemical compounds in the oral cavity. Information derived from taste receptor cells, such as sweet, bitter, salty, sour and umami is important for evaluating the quality of food components. Among five basic taste qualities, sweet taste is very attractive for animals and influences food intake. Recent studies have demonstrated that sweet taste sensitivity in taste receptor cells would be affected by leptin and endocannabinoids. Leptin is an anorexigenic mediator that reduces food intake by acting on leptin receptor Ob-Rb in the hypothalamus. Endocannabinoids such as anandamide [N-arachidonoylethanolamine (AEA)] and 2-arachidonoyl glycerol (2-AG) are known as orexigenic mediators that act via cannabinoid receptor 1 (CB₁) in the hypothalamus and limbic forebrain to induce appetite and stimulate food intake. At the peripheral gustatory organs, leptin selectively suppresses and endocannabinoids selectively enhance sweet taste sensitivity via Ob-Rb and CB₁ expressed in sweet sensitive taste cells. Thus leptin and endocannabinoids not only regulate food intake via central nervous systems but also modulate palatability of foods by altering peripheral sweet taste responses. Such reciprocal modulation of leptin and endocannabinoids on peripheral sweet sensitivity may play an important role in regulating energy homeostasis.     

Palatability of stereoisomers and other amino acid derivatives to fish

Using a behavioral approach, it was shown that stereoisomers and other derivatives of amino acids (Ala, Glu, Gln; 0.1–0.01 М) have different palatability to fish (three-spined stickleback Gasterosteus aculeatus). The palatability of L-α-Ala is higher than of D-α-Ala or L-β-Ala, however, L-Glu and D-Glu equally increase the uptake of agar-agar pellets. L-Glu-Na has no stimulatory effect, probably, due to carnivorous feeding type in the three-spined stickleback. Palatabilities of L-Gln and L-Gln-HCl differ considerably. It is assumed that the influence of the configuration and structure of molecules on the palatability of amino acids to fish, as well as their taste preferences, are species-specific. The diversity of taste properties not only of L-, but also D-isomers of amino acids may matter in choosing adequate food objects in fish. Fish feeding behavior during oral sensory testing of artificial pellets, containing amino acids or their derivatives, obeys two alternative stereotypes, differing in the number of repeated manipulations with pellets and duration of the pellet retention time.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

Evaluating the palatability of fermented foods

ABSTRACT

The present review deal with the novel studies which present possibility of generating a novel sensory evaluation instrument for describing comprehensive food palatability. These studies suggest the palatability can be dissected into its componential subdomains and the subdomains in turn reconstitute comprehensive palatability with evaluation of the quantitative contribution of each subdomain. The studies suggest the novel instrument is useful for comprehensive evaluation of palatability of multifarious fermented foods.     

Diet palatability and growth efficiency: Evidence for a physiological interrelationship in rats

The total food intake and growth efficiency of growing rats were not affected by the feeding of a mild protein restricted (10%) diet containing an aversive taste stimulus. However, growing rats fed the same diet for a period of 18 days, suffered an inhibition of growth efficiency if the taste character of the diet was changed daily by the addition of a single but different aversive stimulus. For a period of time (9 days), these changes in diet palatability did not affect the total food intake. Rats fed diets containing a combination of the aversive taste changes and commercial soybean trypsin inhibitors, suffered an additional inhibition of growth efficiency. It is postulated that these manipulations in diet palatability interfered with digestive or metabolic processes.     

BMI Modulates Calorie-Dependent Dopamine Changes in Accumbens from Glucose Intake

Objective

Dopamine mediates the rewarding effects of food that can lead to overeating and obesity, which then trigger metabolic neuroadaptations that further perpetuate excessive food consumption. We tested the hypothesis that the dopamine response to calorie intake (independent of palatability) in striatal brain regions is attenuated with increases in weight.

Method

We used positron emission tomography with [¹¹C]raclopride to measure dopamine changes triggered by calorie intake by contrasting the effects of an artificial sweetener (sucralose) devoid of calories to that of glucose to assess their association with body mass index (BMI) in nineteen healthy participants (BMI range 21–35).

Results

Neither the measured blood glucose concentrations prior to the sucralose and the glucose challenge days, nor the glucose concentrations following the glucose challenge vary as a function of BMI. In contrast the dopamine changes in ventral striatum (assessed as changes in non-displaceable binding potential of [¹¹C]raclopride) triggered by calorie intake (contrast glucose – sucralose) were significantly correlated with BMI (r = 0.68) indicating opposite responses in lean than in obese individuals. Specifically whereas in normal weight individuals (BMI <25) consumption of calories was associated with increases in dopamine in the ventral striatum in obese individuals it was associated with decreases in dopamine.

Conclusion

These findings show reduced dopamine release in ventral striatum with calorie consumption in obese subjects, which might contribute to their excessive food intake to compensate for the deficit between the expected and the actual response to food consumption.     

Changes in nectar concentration: how quickly do whitebellied sunbirds (Cinnyris talatala) adjust feeding patterns and food intake?

Nectarivorous birds encounter varying nectar concentrations while foraging on different food plants and must adjust their consumption to maintain constant energy intake. We determined how rapidly captive whitebellied sunbirds (Cinnyris talatala) adjust their volumetric intake and feeding patterns after changes in diet concentration. On four consecutive days, birds were fed sucrose diets alternating between a standard diet of 16% w/w and test diets of 2.5, 8.5, 16 or 30% w/w, respectively, for 1.5 h periods. Feeding events were recorded with an infrared photo-detection system and food intake and body mass were monitored continuously by electronic balances interfaced to a computer. Generally, birds demonstrated a measurable increase in feeding frequency and food intake within 10 min after a decrease in sucrose concentration. However, individuals responded differently to the most dilute diet (2.5%): while most increased their food intake, others stopped feeding for a short while, appearing to dislike this diet. Furthermore, the number and duration of feeding events increased in the first 5 min after the switch from 2.5% back to 16%, as the birds attempted to compensate for previous reduced sugar intake. Daily sugar intake was lower when birds alternated between 2.5 and 16% diets than on other test days, but birds were able to maintain body mass, presumably through behavioural adjustments.     

Altered default network activity in obesity

The regulation of energy intake is a complex process involving the integration of homeostatic signals and both internal and external sensory inputs. To better understand the neurobiology of this process and how it may be dysfunctional in obesity, this study examined activity of the brain's "default network" in reduced-obese (RO) as compared to lean individuals. The default network is a group of functionally connected brain regions thought to play an important role in internally directed cognitive activity and the interplay between external and internal sensory processing. Functional magnetic resonance imaging was performed in 24 lean and 18 RO individuals in the fasted state after 2 days of eucaloric energy intake and after 2 days of 30% overfeeding in a counterbalanced design. Scanning was performed while subjects passively viewed images of food and nonfood objects. Independent component analysis was used to identify the default network component. In the eucaloric state, greater default network activity was observed in RO compared to lean individuals in the lateral inferior parietal and posterior cingulate cortices. Activity was positively correlated with appetite. Overfeeding resulted in increased default network activity in lean but not RO individuals. These findings suggest that the function of the default network, a major contributor to intrinsic neuronal activity, is altered in obesity and/or obese-prone individuals. Future studies of the network's function and its relationship to other brain networks may improve our understanding of the mechanisms and treatment of obesity.     

Unequal competitor ideal free distribution in fish?

Key predictions of unequal competitor ideal free distribution models were tested using a continuous input situation. Ten individually identifiable cichlid fish competed for food items at either end of their tank. Their distribution fitted the predictions of the equal competitor, continuous input ideal free model almost perfectly. However, examination of individual intakes revealed significant variation in individual success and relative competitive ability between patches. Contrary to expectations, fish did not exclusively use the patch where their intake was higher, although individuals experiencing greater differences in intake rate between patches were more selective. We found no evidence for a truncated distribution or even a correlation between competitive ability and patch quality. Changing the input regime to reduce competition did not produce a decrease in the range of intake rates between individuals. This study indicates the value of future empirical and theoretical work on how relative competitive ability varies with the nature of the foraging environment.     

Gene expression profiling of cranial sensory ganglia that transmit food intake stimuli

Peripheral cranial sensory nerves projecting into the oral cavity receive food intake stimuli and transmit sensory signals to the central nervous system. They are derived from four cranial sensory ganglia, trigeminal, geniculate, petrosal, and nodose ganglia, each of which contains multiple kinds of sensory neurons with different cell morphologies and neuronal properties. We investigated the complex properties of these neurons from the viewpoint of gene expression using DNA microarrays. The 498 genes were selected from a total of 8,740 genes as showing tissue-dependent expression on the microarray by hierarchical cluster analysis, in which several genes known to be differentially expressed in cranial sensory ganglia are included. This suggests that DNA microarray cluster analysis revealed a number of characteristic genes for sensory neurons in these ganglia. Among the selected 498 genes, 44 genes are associated with neurotransmission, such as neuropeptides, their receptors, and vesicle transport, and 26 are ion channels regulating membrane potentials. The identification of a number of genes related directly to neural properties indicates that these sensory ganglia contain heterogeneous types of neurons with different neural properties.     

Attenuated feeding responses to circadian and palatability cues in mice lacking neuropeptide Y

Neuropeptide Y (NPY) is a potent orexigenic peptide that is implicated in the feeding response to a variety of stimuli. The current studies employed mice lacking NPY (Npy−/−) and their wild-type (Npy+/+) littermates to investigate the role of this peptide in the feeding response to circadian and palatability cues. To investigate the response to a circadian stimulus, we assessed food intake during the 4-h period following dark onset, a time of day characterized by maximal rates of food consumption. Compared to Npy+/+ controls, intake of Npy−/− mice was reduced by 33% during this period (0.6 ± 0.1 g versus 0.9 ± 0.1 g; p ≤ 0.05). In contrast, intake did not differ between genotypes when measured over a 24-h period (3.7 ± 0.2 g versus 3.5 ± 0.3 g; p = ns). Furthermore, reduced dark cycle 4 h food intake in Npy−/− mice was not evident after a 24-h fast (1.4 ± 0.1 g for both genotypes; p = ns), despite a pronounced delay in the initiation of feeding (636 ± 133 s versus 162 ± 29 s; p ≤ 0.05). To investigate the role of NPY in the feeding response to palatability cues, mice were presented with a highly palatable diet (HP) for 1 h each day (in addition to having ad libitum access to chow) for 18 days. Npy+/+ mice rapidly increased daily HP intake such that by the end of the first week, they derived a substantial fraction of daily energy from this source (41 ± 3%). By comparison, HP intake was markedly reduced in Npy−/− mice during the first week (24 ± 7% of daily energy intake, p ≤ 0.05 versus Npy+/+), although it eventually increased (by Day 9) to values comparable to those of Npy+/+ controls. These experiments suggest that NPY contributes to the mechanism whereby food intake increases in response to circadian and palatability cues and that mechanisms driving food intake in response to these stimuli differ from those activated by energy restriction.     

Acute stress-related changes in eating in the absence of hunger

Obesity results from chronic deregulation of energy balance, which may in part be caused by stress. Our objective was to investigate the effect of acute and psychological stress on food intake, using the eating in the absence of hunger paradigm, in normal and overweight men and women (while taking dietary restraint and disinhibition into account). In 129 subjects (BMI = 24.5 +/- 3.4 kg/m(2) and age = 27.6 +/- 8.8 years), scores were determined on the Three Factor Eating Questionnaire (dietary restraint = 7.2 +/- 4.4; disinhibition = 4.5 +/- 2.6; feeling of hunger = 3.9 +/- 2.6) and State-Trait Anxiety Inventory (trait score = 31.7 +/- 24.2). In a randomized crossover design, the "eating in absence of hunger" protocol was measured as a function of acute stress vs. a control task and of state anxiety scores. Energy intake from sweet foods (708.1 kJ vs. 599.4 kJ, P < 0.03) and total energy intake (965.2 kJ vs. 793.8 kJ, P < 0.01) were significantly higher in the stress condition compared to the control condition. Differences in energy intake between the stress and control condition were a function of increase in state anxiety scores during the stress task (Delta state anxiety scores) (R(2) = 0.05, P < 0.01). This positive relationship was stronger in subjects with high disinhibition scores (R(2) = 0.12, P < 0.05). Differences in state anxiety scores were a function of trait anxiety scores (R(2) = 0.07, P < 0.05). We conclude that acute psychological stress is associated with eating in the absence of hunger, especially in vulnerable individuals characterized by disinhibited eating behavior and sensitivity to chronic stress.     

Social information, social feeding, and competition in group-living goats (Capra hircus)

There are both benefits (e.g., social information) and costs(e.g., intraspecific competition) for individuals foraging ingroups. To ascertain how group-foraging goats (Capra hircus)deal with these trade-offs, we asked 1) do goats use socialinformation to make foraging decisions and 2) how do they adjusttheir intake rate in light of having attracted by other groupmembers? To establish whether goats use social information,we recorded their initial choice of different quality food patcheswhen they were ignorant of patch quality and when they couldobserve others foraging. After determining that goats use socialinformation, we recorded intake rates while they fed alone andin the presence of potential competitors. Intake rate increasedas the number of competitors increased. Interestingly, lonegoats achieved an intake rate that was higher than when onecompetitor was present but similar to when two or more competitorswere present. Faster intake rates may allow herbivores to ingesta larger portion of the available food before competing groupmembers arrive at the patch. This however, does not explainthe high intake rates achieved when the goats were alone. Weprovide 2 potential explanations: 1) faster intake rates area response to greater risk incurred by lone individuals, theloss of social information, and the fear of being left behindby the group and 2) when foraging alone, intake rate is no longera trade-off between reducing competition and acquiring socialinformation. Thus, individuals are able to feed close to theirmaximum rate.     

Alteration of sweet taste in high-fat diet induced obese rats after 4 weeks treatment with exenatide

Exenatide, a glucagon-like peptide-1 (GLP-1) receptor agonist, is effective in inducing weight loss. The exact mechanisms are not fully understood. Reduced appetite and food intake may play important roles. Sweet taste contributes to food palatability, which promotes appetite. Interestingly, GLP-1 and its receptor are expressed in the taste buds of rodents and their interaction has an effect on mediating sweet taste sensitivity. Our aim was to investigate whether sweet taste will be changed after long term treatment with exenatide. The results showed that high-fat diet induced obese rats (HF-C) presented metabolic disorders in food intake, body weight, blood glucose and lipid metabolism compared with long term exenatide treated obese rats (EX) and normal chow fed control rats (NC). Meanwhile, greater preference for sweet taste was observed in HF-C rats but not in EX rats. Compared with NC rats, brain activities induced by sweet taste stimulation were stronger in HF-C rats, however these stronger activities were not found in EX rats. We further found reduced sweet taste receptor T1R3 in circumvallte taste buds of HF-C rats, while GLP-1 was increased. Besides, serum leptin was evaluated in HF-C rats with decreased leptin receptor expressed in taste buds. These changes were not observed in EX rats, which suggest them to be the underlying hormone and molecular mechanisms responsible for alterations in sweet taste of HF-C rats and EX rats. In summary, our results suggest that long term treatment with exenatide could benefit dietary obese rats partially by reversing sweet taste changes.