Visual-gustatory interaction: orbitofrontal and insular cortices mediate the effect of high-calorie visual food cues on taste pleasantness

Vision provides a primary sensory input for food perception. It raises expectations on taste and nutritional value and drives acceptance or rejection. So far, the impact of visual food cues varying in energy content on subsequent taste integration remains unexplored. Using electrical neuroimaging, we assessed whether high- and low-calorie food cues differentially influence the brain processing and perception of a subsequent neutral electric taste. When viewing high-calorie food images, participants reported the subsequent taste to be more pleasant than when low-calorie food images preceded the identical taste. Moreover, the taste-evoked neural activity was stronger in the bilateral insula and the adjacent frontal operculum (FOP) within 100 ms after taste onset when preceded by high- versus low-calorie cues. A similar pattern evolved in the anterior cingulate (ACC) and medial orbitofrontal cortex (OFC) around 180 ms, as well as, in the right insula, around 360 ms. The activation differences in the OFC correlated positively with changes in taste pleasantness, a finding that is an accord with the role of the OFC in the hedonic evaluation of taste. Later activation differences in the right insula likely indicate revaluation of interoceptive taste awareness. Our findings reveal previously unknown mechanisms of cross-modal, visual-gustatory, sensory interactions underlying food evaluation.     

Modulation of taste sensitivity by GLP-1 signaling

In many sensory systems, stimulus sensitivity is dynamically modulated through mechanisms of peripheral adaptation, efferent input, or hormonal action. In this way, responses to sensory stimuli can be optimized in the context of both the environment and the physiological state of the animal. Although the gustatory system critically influences food preference, food intake and metabolic homeostasis, the mechanisms for modulating taste sensitivity are poorly understood. In this study, we report that glucagon-like peptide-1 (GLP-1) signaling in taste buds modulates taste sensitivity in behaving mice. We find that GLP-1 is produced in two distinct subsets of mammalian taste cells, while the GLP-1 receptor is expressed on adjacent intragemmal afferent nerve fibers. GLP-1 receptor knockout mice show dramatically reduced taste responses to sweeteners in behavioral assays, indicating that GLP-1 signaling normally acts to maintain or enhance sweet taste sensitivity. A modest increase in citric acid taste sensitivity in these knockout mice suggests GLP-1 signaling may modulate sour taste, as well. Together, these findings suggest a novel paracrine mechanism for the regulation of taste function.     

RETRACTED: SENSORY SUGGESTIVENESS AND LABELING: DO SOY LABELS BIAS TASTE?1

Can labels suggestively influence sensory perceptions and taste? Using a “ Phantom Ingredient” taste test, we show that the presence or absence of a labeled ingredient (soy) and the presence or absence of a health claim negatively bias taste perceptions toward a food erroneously thought to contain soy. We found a label highlighting soy content made health claims believable but negatively influenced perceptions of taste for certain segments of consumers. Our results and discussion provide better direction for researchers who work with ingredient labeling as well as for those who work with soybean products.     

NEUROPHYSIOLOGY AND HUMAN TASTE SENSATIONS

Taste sensations are of primary importance in food flavor. Any attempt to synthesize chemically the flavor of a natural food involves mainly taste active compounds. Many distinct taste sensations can be identified as associated with food compounds. Thirteen different taste sensations are discussed herein. These different taste sensations are differentiated on the basis of stimulus chemistry and peripheral nerve conveying the taste information. Neurophysiological examination of the peripheral nerves involved in taste reveals that the sensory neurons can, in any species, be subdivided into distinct neural groups. These different neural groups respond to distinct classes of chemicals and often display different neurophysiological characteristics. Altogether in four different species, nine functional neural taste groups can be distinguished. In many cases, these neural groups can be taken as analogs for the neural groups assumed to underly human taste sensations. Distinct human taste sensations can be considered to arise from the excitation or inhibition of different neural groups. For certain human taste sensations there are no animal neural analog groups; and for certain neural groups there are no analog human sensations.     

Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion

Complementary neurophysiological recordings in macaques and functional neuroimaging in humans show that the primary taste cortex in the rostral insula and adjoining frontal operculum provides separate and combined representations of the taste, temperature, and texture (including viscosity and fat texture) of food in the mouth independently of hunger and thus of reward value and pleasantness. One synapse on, in the orbitofrontal cortex, these sensory inputs are for some neurons combined by learning with olfactory and visual inputs. Different neurons respond to different combinations, providing a rich representation of the sensory properties of food. The representation of taste and other food-related stimuli in the orbitofrontal cortex of macaques is found from its lateral border throughout area 13 to within 7 mm of the midline, and in humans the representation of food-related and other pleasant stimuli is found particularly in the medial orbitofrontal cortex. In the orbitofrontal cortex, feeding to satiety with one food decreases the responses of these neurons to that food, but not to other foods, showing that sensory-specific satiety is computed in the primate (including human) orbitofrontal cortex. Consistently, activation of parts of the human orbitofrontal cortex correlates with subjective ratings of the pleasantness of the taste and smell of food. Cognitive factors, such as a word label presented with an odour, influence the pleasantness of the odour, and the activation produced by the odour in the orbitofrontal cortex. Food intake is thus controlled by building a multimodal representation of the sensory properties of food in the orbitofrontal cortex, and gating this representation by satiety signals to produce a representation of the pleasantness or reward value of food which drives food intake. A neuronal representation of taste is also found in the pregenual cingulate cortex, which receives inputs from the orbitofrontal cortex, and in humans many pleasant stimuli activate the pregenual cingulate cortex, pointing towards this as an important area in motivation and emotion.     

Effects of the long-term anosmia combined with vision deprivation on the taste sensitivity and feeding behavior of the rainbow trout <Emphasis Type="Italic">Parasalmo</Emphasis> (=<Emphasis Type="Italic">Oncorhynchus</Emphasis>) <Emphasis Type="Italic">mykiss</Emphasis>

We compared taste preferences, taste sensitivity, and behavior in testing food objects in the group of intact and two groups of sensory deprived rainbow trout Oncorhynchus mykiss yearlings. We demonstrated that long-term anosmia (for 9 months), as well as anosmia (for 9 months) combined with enucleation (object vision deprivation for 4 months), does not change the taste preference of fish for the agar pellets containing amino acids (L-alanine, L-proline, L-histidine, or glycine; 0.1 M). For all groups of fish, the threshold L-alanine concentration in pellets that caused a significant increase in consumption is 0.01 M. We showed that sensory deprived fish change their behavior of gustatory testing, namely, the rate of repeated snaps decreases as well as the pellet retention time in the mouth cavity. These results demonstrate that long-term anosmia combined with a partial vision deprivation does not significantly change the taste preferences and sensitivity in the fish that have no external taste buds. However, the observed reduction in the testing time of food objects and other changes in fish feeding behavior may suggest some functional alterations in the intraoral sensory systems (gustatory and/or tactile).     

Comparing sensory experiences across individuals: recent psychophysical advances illuminate genetic variation in taste perception

Modern psychophysics has traveled considerably beyond the threshold measures that dominated sensory studies in the first half of this century. Current methods capture the range of perceived intensity from threshold to maximum and promise to provide increasingly accurate comparisons of perceived intensities across individuals. The application of new psychophysical tools to genetic variation in taste allowed us to discover supertasters, individuals who live in particularly intense taste worlds. Because of the anatomy of the taste system, supertasters feel more burn from oral irritants like chili peppers, more creaminess/ viscosity from fats and thickeners in food and may also experience more intense oral pain. Not surprisingly, these sensory differences influence food choices and thus health. A discussion of the milestones on the road to understanding genetic variation in taste must include discussion of some potholes as well. Often our failures have been as instructive as our successes in the effort to evaluate the impact of genetic variation in taste.     

Identification of neurons responsible for feeding behavior in the Drosophila brain

Drosophila melanogaster feeds mainly on rotten fruits,which contain many kinds of sugar.Thus,the sense of sweet taste has evolved to serve as a dominant regulator and driver of feeding behavior.Although several sugar receptors have been described,it remains poorly understood how the sensory input is transformed into an appetitive behavior.Here,we used a neural silencing approach to screen brain circuits,and identified neurons labeled by three Gal4 lines that modulate Drosophila feeding behavior.These three Gal4 lines labeled neurons mainly in the suboesophageal ganglia(SOG),which is considered to be the fly’s primary taste center.When we blocked the activity of these neurons,flies decreased their sugar consumption significantly.In contrast,activation of these neurons resulted in enhanced feeding behavior and increased food consumption not only towards sugar,but to an array of food sources.Moreover,upon neuronal activation,the flies demonstrated feeding behavior even in the absence of food,which suggests that neuronal activation can replace food as a stimulus for feeding behavior.These findings indicate that these Gal4-labeled neurons,which function downstream of sensory neurons and regulate feeding behavior towards different food sources is necessary in Drosophila feeding control.     

Taste recognition: food for thought

The ability to identify food that is nutrient-rich and avoid toxic substances is essential for an animal's survival. Although olfaction and vision contribute to food detection, the gustatory system acts as a final checkpoint control for food acceptance or rejection behavior. Recent studies with model organisms such as mice and Drosophila have identified candidate taste receptors and examined the logic of taste coding in the periphery. Despite differences in terms of gustatory anatomy and taste-receptor families, these gustatory systems share a basic organization that is different from other sensory systems. This review will summarize our current understanding of taste recognition in mammals and Drosophila, highlighting similarities and raising several as yet unanswered questions.     

SENSORY INTERACTIONS IN MIXTURES

Psychological studies have assessed the intensity of simple sensory mixtures, both in taste and olfaction. In taste mixtures, suppression or partial masking among the components is often observed. An analogous result is often found in odor mixtures, counteraction of one component in the presence of a second odor. These effects, particularly taste suppression, are also observed in food systems. Interactions between sensory modalities are far more complex, ranging from inhibition of taste and odor sensations by trigeminal irritation, to relative independence of tastes from odor stimulation and independence of odors from tastes.     

The human bitter taste receptor, hTAS2R16, discriminates slight differences in the configuration of disaccharides

Sweetness and bitterness are key determinants of food acceptance and rejection, respectively. Sugars, such as sucrose and fructose, are generally recognized as sweet. However, not all sugars are sweet, and even anomers may have quite different tastes. For example, gentiobiose is bitter, whereas its anomer, isomaltose, is sweet. Despite this unique sensory character, the molecular basis of the bitterness of gentiobiose remains to be clarified. In this study, we used calcium imaging analysis of human embryonic kidney 293T cells that heterologously expressed human taste receptors to demonstrate that gentiobiose activated hTAS2R16, a bitter taste receptor, but not hT1R2/hT1R3, a sweet taste receptor. In contrast, isomaltose activated hT1R2/hT1R3. As a result, these anomers elicit different taste sensations. Mutational analysis of hTAS2R16 also indicated that gentiobiose and β-d-glucopyranosides, such as salicin share a common binding site of hTAS2R16.     

A fly rhodopsin sheds light on thermal taste

In their recent paper, Li and colleagues discover that cold food tastes less sweet to flies, in part by activating bitter sensory neurons through a rhodopsin-dependent mechanism [1]. This work establishes temperature as an important variable in understanding fly taste processing and adds diversity to the sensory roles for rhodopsin receptors.     

Food perception with age and its relationship to pleasantness

Differences between elderly subjects (n = 46, 61-86 years) and young subjects (n = 36, 18-25 years) in food perception and food liking were investigated. Intensity and liking ratings were assessed for custard dessert, in which flavor enrichment, textural change, and irritant addition were incorporated as strategies to compensate for sensory losses with increasing age. The sensory acuity (taste, olfaction, irritation, chewing efficiency) of both young and elderly subjects was measured with the help of different sensitivity tests. The elderly perceived the custards differently from the young, mainly as less intense in flavor (cherry/vanilla) and less intense in creaminess/swallowing effort. Several of the observed interaction effects were different for the elderly and the young. The majority of these differences manifested as lower intensity slopes for the elderly. Losses in sensitivity to taste and to olfactory and trigeminal stimuli as well as a reduced chewing efficiency were observed on average for the elderly compared with the young. Furthermore, subgroups of the elderly were observed in which the compensatory strategies flavor enrichment, textural change, and irritant addition led to an increase in food liking. However, these subgroups did not differ in their sensory acuity. The present study does not support the assumption that age-associated changes in food perception-caused by losses in sensory acuity-inevitably reduce the food liking of the elderly.     

Fat taste in humans: Sources of within- and between-subject variability

Non-esterified fatty acids (NEFA) are reportedly detectable through taste mechanisms in the human oral cavity. However, wide variability has been observed in NEFA taste sensitivity between and within subjects as well as across research groups. Some of this variability may be due to the hydrophobic nature of the NEFA and the methods used to make stimuli emulsions. As NEFA are poorly soluble in water, emulsification is necessary for delivery of stimuli to taste receptors. However, properties of emulsions may also be detected by somatosensory cues complicating attribution of sensory findings to taste. Additionally, learning (improved test performance) has been observed when using traditional tests for measuring sensitivity to NEFA, which may contribute greatly to within-subject variability if not standardized. Factors such as sex, diet, and BMI have been proposed to affect NEFA taste sensitivity, but the degree to which these individual factors influence NEFA detection thresholds remains to be fully established. Improved knowledge of stimulus properties and individual sensory capabilities will be needed to further evaluate the posited taste component to human oral fat detection. Progress in this area should facilitate the translation of findings on how NEFA taste may contribute to or reflect food choice and chronic disease risk.     

Taste receptors in the gastrointestinal tract III. Salty and sour taste: sensing of sodium and protons by the tongue

Taste plays an essential role in food selection and consequently overall nutrition. Because salt taste is appetitive, humans ingest more salt than they need. Acids are the source of intrinsically aversive sour taste, but in mixtures with sweeteners they are consumed in large quantities. Recent results have provided fresh insights into transduction and sensory adaptation for the salty and sour taste modalities. The sodium-specific salt taste receptor is the epithelial sodium channel whereas a nonspecific salt taste receptor is a taste variant of the vanilloid receptor-1 nonselective cation channel, TRPV1. The proximate stimulus for sour taste is a decrease in the intracellular pH of a subset of acid-sensing taste cells, which serves as the input to separate transduction pathways for the phasic and tonic parts of the sour neural response. Adaptation to sour arises from the activation of the basolateral sodium-hydrogen exchanger isoform-1 by an increase in intracellular calcium that sustains the tonic phase of the sour taste response.     

Brain mechanisms underlying flavour and appetite

Complementary neurophysiological recordings in macaques and functional neuroimaging in humans show that the primary taste cortex in the rostral insula and adjoining frontal operculum provides separate and combined representations of the taste, temperature and texture (including viscosity and fat texture) of food in the mouth independently of hunger and thus of reward value and pleasantness. One synapse on, in the orbitofrontal cortex, these sensory inputs are for some neurons combined by learning with olfactory and visual inputs. Different neurons respond to different combinations, providing a rich representation of the sensory properties of food. In the orbitofrontal cortex, feeding to satiety with one food decreases the responses of these neurons to that food, but not to other foods, showing that sensory-specific satiety is computed in the primate (including human) orbitofrontal cortex. Consistently, activation of parts of the human orbitofrontal cortex correlates with subjective ratings of the pleasantness of the taste and smell of food. Cognitive factors, such as a word label presented with an odour, influence the pleasantness of the odour and the activation produced by the odour in the orbitofrontal cortex. These findings provide a basis for understanding how what is in the mouth is represented by independent information channels in the brain; how the information from these channels is combined; and how and where the reward and subjective affective value of food is represented and is influenced by satiety signals. Activation of these representations in the orbitofrontal cortex may provide the goal for eating, and understanding them helps to provide a basis for understanding appetite and its disorders.     

Sorting food from stones: the vagal taste system in Goldfish, Carassius auratus

The sense of taste, although a relatively undistinguished sensory modality in most mammals, is a highly developed sense in many fishes, e.g., catfish, gadids, and carps including goldfish. In these species, the amount of neural tissue devoted to this modality may approach 20% of the entire brain mass, reflecting an enormous number of taste buds scattered across the external surface of the animal as well as within the oral cavity. The primary sensory nuclei for taste form a longitudinal column of nuclei along the dorsomedial surface of the medulla. Within this column of gustatory nuclei, the sensory system is represented as a fine-grain somatotopic map, with external body parts being represented rostrally within the column, and oropharyngeal surfaces being represented caudally. Goldfish have a specialization of the oral cavity, the palatal organ, which enables them to sort food particles from particulate substrate material such as gravel. The palatal organ taste information reaches the large, vagal lobe with a complex laminar and columnar organization. This lobe also supports a radially-organized reflex system which activates the musculature of the palatal organ to effect the sorting operation. The stereotyped, laminated structure of this system in goldfish has facilitated studies of the circuitry and neurotransmitter systems underlying the goldfish’s ability to sort food from stones.     

Peptide regulators of peripheral taste function

The peripheral sensory organ of the gustatory system, the taste bud, contains a heterogeneous collection of sensory cells. These taste cells can differ in the stimuli to which they respond and the receptors and other signaling molecules they employ to transduce and encode those stimuli. This molecular diversity extends to the expression of a varied repertoire of bioactive peptides that appear to play important functional roles in signaling taste information between the taste cells and afferent sensory nerves and/or in processing sensory signals within the taste bud itself. Here, we review studies that examine the expression of bioactive peptides in the taste bud and the impact of those peptides on taste functions. Many of these peptides produced in taste buds are known to affect appetite, satiety or metabolism through their actions in the brain, pancreas and other organs, suggesting a functional link between the gustatory system and the neural and endocrine systems that regulate feeding and nutrient utilization.     

Phospholipase C-beta 2 as a mammalian taste signaling marker is expressed in the multiple gustatory tissues of medaka fish, Oryzias latipes

Phospholipase C-beta 2 (PLC-beta 2) is a key enzyme in mammalian taste signal transduction. To analyze the taste system in fishes at molecular level, we cloned mfplc-beta 2 as a medaka fish homologue of PLC-beta 2. In situ hybridization analysis revealed that mfplc-beta 2 is expressed in the lip and branchial region where chemosensory tissues are distributed. Immunohistochemical detection of nerve fibers near the mfplc-beta 2 positive cells suggests the characteristic of peripheral sensory cells. These results suggest that mfplc-beta 2 is expressed in the gustatory sensory cells of medaka. This may provide a molecular basis for the taste reception at multiple tissues in fish species.     

The taste system in fishes and the effects of environmental variables

The adaptability of the taste system in fish has led to a large variety in taste bud morphology, abundance and distribution, as well as in taste physiology characteristics in closely related species with different modes of life and feeding ecology. However, the modifications evoked in the sense of taste, or gustation, particularly during ontogeny when fishes are subject to different environmental variables, remain poorly studied. This review paper focusses on current knowledge to show how plastic and resistant the taste system in fishes is to various external factors, linked to other sensory inputs and shifts in physiological state of individuals. Ambient water temperature is fundamental to many aspects of fish biology and taste preferences are stable to many substances, however, the taste-cell turnover rate strongly depends on water temperature. Taste preferences are stable within water salinity, which gives rise to the possibility that the taste system in anadromous and catadromous fishes will only change minimally after their migration to a new environment. Food-taste selectivity is linked to fish diet and to individual feeding experience as well as the motivation to feed evoked by attractive (water extracts of food) and repellent (alarm pheromone) odours. In contrast, starvation leads to loss of aversion to many deterrent substances, which explains the consumption by starving fishes of new objects, previously refused or just occasionally consumed. Food hardness can significantly modify the final feeding decision to swallow or to reject a grasped and highly palatable food item. Heavy metals, detergents, aromatic hydrocarbons and other water contaminants have the strongest and quickest negative effects on structure and function of taste system in fish and depress taste perception and ability of fishes to respond adequately to taste stimuli after short exposures. Owing to phenotypic plasticity, the taste system can proliferate and partially restore the ability of fishes to respond to food odour after a complete loss of olfaction. In general, the taste system, especially its functionality, is regarded as stable over the life of a fish despite any alteration in their environment and such resistance is vital for maintaining physiological homeostasis.