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J Nutr Food Sci.Author manuscript; available in PMC 2018 on May 14.
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Published online March 31, 2018. doi:10.4172/2155-9600.1000686
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The publisher's final edited version of this article is available atJ Nutr Food Sci
Abstract
Taste is important in guiding food choices and motivating food intake. The senses of taste are the taste buds, which convert taste stimuli into neural signals. It has been reported that chickens have a low number of taste buds and thus low taste sharpness. However, recent studies indicate that chickens have a well-developed gustatory system, and the reported number and distribution of taste buds may have been significantly underestimated. Chickens, as a proven animal model for research, are also the most important animal species in the poultry industry. A clear understanding of taste organ formation and the effects of taste perception on diet and feeding practices is therefore important for improving livestock husbandry strategies. In this review, we provide an update on recent findings in the field of chicken taste buds and taste perception, indicating that the chicken gustatory organ is better developed than previously thought and could serve as an ideal system for interdisciplinary studies including organogenesis, regenerative medicine, diet and nutritional value. selection.
Keyword:Chicken, flavor, poultry, feed, nutrition
Introduction
The sense of taste in vertebrates is conserved - most species have a well-developed gustatory system consisting of gustatory organs, the innervating nerves and the central nervous system. In this review we will focus on the sense of taste in chickens, including their senses and behavioral responses.
Recent studies have increased our understanding of basic information about the number, distribution, structure, and development of chicken taste buds. By using molecular markers to label chicken taste buds in the oral epithelial layer, many more taste buds have been observed. This suggests that chickens have a better developed gustatory system and therefore a greater influence of taste on their feeding behavior than previously assumed.
Sensory organs for taste in chickens
The senses of taste are taste buds, which detect different types of flavor compounds and convert taste stimuli into neural signals sent to the brain for taste perception. Among different species, the distribution of taste buds varies. For example, mammalian taste buds are located primarily in the tongue, although they are also seen in the soft palate, epiglottis, pharynx, larynx, and uvula.1-4]. In contrast, the gustatory system of birds is a prominent example of a non-linguistic gustatory system. The taste buds of chickens differ in many ways from the taste buds of mammals.
The number, distribution and structure of the taste buds
It was originally reported that chickens have no taste buds [5] and later about 70 taste buds were found in the oral cavity [6]. This number is low compared to mammals, e.g. rats (~1000 taste buds), humans (~10,000 taste buds) [1] and cattle, which have about 15,000-20,000 taste buds [7]. Further research has shown that chickens have a larger number of taste buds, ranging in number from an average of 240 to 360, depending on the breed. broiler chickens have more taste buds compared to the laying hen type [8-10]. Furthermore, our recent studies have shown that the number of taste buds varies between lines in chicks of the same type (broiler type) at P3, i.e. females have more taste buds on the floor of the oral cavity than males and females. male line men [11].
Chicken taste buds are present in both the anterior and posterior parts of the oral cavity, mainly divided into three parts of the oral epithelium: the palate (~69%) (orifice region of the anterior maxillary gland, mid-palatal papilla region and posterior region), floor of the oral cavity (anterior mandibular region) (~29%) and posterior ventrolateral areas of the keratinized anterior tongue and posterior part of the tongue (region posterior to the lingual column) (~2%) [8,9]. In the oral epithelium, taste buds are mainly located near salivary gland orifices (>20 μm in diameter) [8,11]. The two clusters of taste buds in the region of the anterior maxillary gland opening of the palate are large and dense, which may be important for immediate detection as soon as food enters the oral cavity. The lower number of lingual taste buds in chickens suggests that the tongue is not the most important taste organ in chickens; rather, it facilitates food processing.
The taste buds of chickens consist of a cluster of specified spindle-shaped cells and are ovoid ("ovoid"), unlike mammals whose taste buds are spherical/bud-shaped. Using 2-photon microscopy in the oral epithelial sheet immunostained with molecular markers, large tube-like taste buds were also observed in the posterior part of the palate.11]. Unlike mammals, chickens do not have specialized structures such as lingual taste buds (i.e. mushroom-shaped, leaf-shaped, circumferential) that house taste buds. The taste buds are embedded in the epithelium and grouped in clusters around the openings of the salivary glands in a rosette pattern.8,11]. Regarding the distribution of the taste buds, we found that the taste buds at the bottom of the oral cavity extend to the lateral border [11], indicating a broader distribution than previously observed.
The previous data on the number and distribution of taste buds were obtained from the observation of taste trails (2–10 μm in diameter) with scanning electron microscopy [8]. Recently, we used molecular markers, α-Gustducin and Vimentin, to label chicken taste buds in the desiccated epithelial layer and found many more taste buds than previously reported [11]. Figures vary by sex, even within the same breed (COBB 500) - male chickens from the female line have more taste buds than females and male chickens from the male line. The male chicks of female-line broilers have up to 500 taste buds in the palate and ~260 in the floor of the oral cavity at P3, which is much higher than the number previously reported by scanning electron microscopy (218 in the palate and 91 in the mouth). floor of the oral cavity) [8]. The ratio of salivary gland orifices to taste buds in chicks has been reported to be approximately 1:2.5, a ratio that does not change with age.9]. However, using molecular markers to label taste buds, larger clusters are observed at the floor of the oral cavity, e.g. 4 buds per average cluster (up to 14) in males and an average of 3 buds in females (up to 9) [11]. The high number of taste buds in chicks implies a better developed gustatory system and possibly a greater than previously recognized gustatory influence on bird feeding behavior.
Previous research has shown that the total number of taste buds in young and adult chickens is similar [12]. However, a more detailed analysis revealed that the number of taste buds and clusters changes with age from P0-P8. For example, the number of taste buds in broiler-type males increases after hatching, peaks at P3, and then decreases at later stages. The continued development of taste buds in chicks after P0 provides a time frame during which taste bud formation and thus taste sensation can be altered in early hatched chicks.11].
Trial bud cell types
As in mammals, the chick taste bud population is histologically heterogeneous.8,13]. In mammals, there are four types of taste bud cells: type I cells (dark), type II cells (light), which are considered "receptor cells", type III (intermediate cells), and type IV cells (basal cells). . Several types of taste buds have been identified in chickens based on ultrastructural studies using transmission electron microscopy.
There are at least four types of taste buds classified based on their appearance, including basal cells, dark cells, light cells, and flattened/intermediate cells.14]. The dark cells, the most common cell type in chicken taste buds, have cytoplasmic extensions (similar to microvilli in mammalian taste buds) and their main function is thought to support the taste buds.15]. In addition, dark cells have dense cytoplasm with scattered chromatin and fewer vesicles. The light cells, similar to type II taste bud cells in mammals, have a less dense cytoplasm but more vesicles compared to dark cells. The intermediate cells have certain characteristics of both light and dark cells.14]. Basal cells, as the name implies, are located in the basal region of the taste buds, have an irregularly shaped nucleus, dense cytoplasm, and are darker than the other cell types.14].
Specific markers for the three types of differentiated taste bud cells in rodents are well characterized, e.g. NTPDase II for type I [16], α-Gustducin all type II [17,18], SNAP25 tot type III [19]. However, there are no established molecular markers to identify the specific taste cell types in chicks, although molecular markers (Vimentin and α-Gustducin) are available to label taste buds.11,20-22].
Development and maintenance of taste buds
Development of the taste buds of chicken
The chick's beak and tongue, the areas where the oral tissues house taste buds, develop at embryonic day (E) 8, and taste buds appear at E17 (Hamburger Hamilton stage 43) as a globular cluster of cells at the base of the epithelium. From E17-18, the cell clusters continue to develop and increase in number, although no pore penetrates the surface of the epithelium. At E19, the taste bud cells elongate and form an ovoid structure with a narrow and shallow taste trail that penetrates the surface of the epithelium.12]. Compared to rodents, chickens' taste buds develop and mature early. before they hatch [23]. In rodents, taste bud development and maturation occurs after birth, and taste bud maturation is completed 2-3 weeks after birth.24].
At E19 the number of taste buds peaks and is reported to remain consistent after hatching in most chicks.12]. It is hypothesized that the number of taste buds in young chicks remained relatively static compared to adult chicks, with no age-related effects on taste bud development.25]. As previously discussed, in Cobb 500 broiler type chicks, the males of the female line continue to develop taste buds after hatching, peaking at P3 and then declining to a stable level.11].
Preserves the taste of chicken
Taste buds are located in the epithelium and contain cells with epithelial properties: they have a short lifespan and undergo constant renewal. It has been suggested that the rate of cell turnover depends on the type, age and location of the taste buds.26,27]. In chickens, the average lifespan of taste buds is shorter compared to other vertebrates reported to date. The lifespan of chicken taste cells in the floor of the oral cavity is on average 3-4 days [26,27], as opposed to 7-14 days in mammals [26,28,29]. The high turnover rate of taste buds requires a strict precursor/stem cell niche to maintain proper gustatory function. Type IV/basal cells are considered one of these stem cell niches. Furthermore, the “edge/perigemmal” cells immediately surrounding the taste buds are highly proliferative, implicitly reflected in their function in cell turnover of the taste buds.
Our recent studies have revealed a population of proliferating cells in chicken taste buds that are predominantly unlabeled by other known markers of chicken taste cells (i.e., Vimentin and α-Gustducin), suggesting that this is a distinct and undifferentiated population of taste cells. This is unique because the taste bud cells in rodents are largely post-mitotic – their proliferating cells are mainly located in the surrounding epithelium [30] and possibly the connective tissue [31]. The unique localization of proliferating cells in chicken taste buds along the basal layer suggests the possibility that taste buds are predominantly independent structures with “built-in” progenitor cells to meet the needs of their large size and rapid turnover. However, proliferating cells also reside in other tissue compartments, such as epithelium and connective tissue, so lineage tracing should be performed to confirm this suspicion.
Regulation of the development and maintenance of the taste buds
Taste organs, like other epithelial appendages, require epithelial-mesenchymal interactions and the involvement of multiple signaling pathways for proper formation. Sonic hedgehog (Shh) and bone morphogenetic protein (BMP) signaling cascades have been identified in avian tongue development.32], where there is a small population of taste buds. The signaling mechanisms underlying chicken taste bud development are largely unknown.
Knowledge about the regulation of taste organ development in rodents can provide us with perspective and be useful for in-depth studies in chickens. In rodents, several molecular pathways have been identified that regulate embryonic tongue development and develop taste buds and taste buds. For example. Hedgehog [33-38], Wnt/β-catenine [39-43] TGF-β/BMP [44-47], right [48-50] fibroblastgroeifactor (FGF) [45,51,52], and Erbb[53-55].
Recently, we used RNA-Seq analysis to map the transcriptomic architecture of gustatory tissue development in chickens.56]. Although chickens have taste buds throughout the oral cavity, including the epithelium of the palate, the floor of the oral cavity, and the posterior tongue, analyzes between the epithelium and the underlying mesenchyme in each tissue showed that the epithelium of the floor of the oral cavity contained the most differentially expressed genes (DEGs) related to taste, including but not limited to GNAT3 and TAS1R3. A deeper analysis of this tissue using areas of the epithelium containing (taste) or not (non-taste) taste buds, as well as the mesenchyme underlying the taste epithelium, revealed components of several pathways involved in organogenesis and which were expressed in different ways. Indeed, TGFβ/BMP, FGF, Notch, SHH, and ERbb signaling cascades were differentially expressed between taste epithelium and taste mesenchyme, implicating the regulatory role of these tissues in taste bud development and maintenance.
In summary, chicken gustatory organs represent an ideal system for multidisciplinary studies, including organogenesis and regenerative medicine, given their many characteristics, as outlined below: (1) a unique distribution pattern in the gustatory tissue of the oral cavity; (2) a much shorter lifespan (-4 days) compared to mammals (-10-12 days in rodents), indicating a more active precursor cell niche and allowing a more efficient way to study taste bud renewal compared to rodent model; (3) similarity to humans in the connective tissue cell marker Vimentin, which is expressed in a large population of taste bud cells, suggesting a similar mechanism underlying the contribution of connective tissue to the taste buds in both organisms; (4) development of new taste buds after hatching, which provides a time window to study the regulation of taste bud development; (5) other beneficial aspects of using chickens as a research model, e.g. ease of in vivo embryo manipulation, high availability and rapid development.
Behavioral responses of chickens to taste stimuli
Chicks respond to taste stimuli immediately after hatching, and newly hatched chicks respond to different taste stimuli and exhibit aversion/acceptance behavior to different tastes [23,57]. Behavioral studies have identified the typical response to tastants including head shaking, beak flicking and tongue/beak movements. In addition, the ability of tastes to send signals to the brain has been analyzed with an electroencephalogram (EEG) [58].
Taste sensitivity in chickens
Taste sensitivity in chickens correlates positively with the total number of taste buds, i.e. the more taste buds, the more sensitive the bitter taste [10,59]. Broiler males are more sensitive to taste stimuli than laying hen males because they have more taste buds [8,9]. There is broad consensus that birds have lower gustatory acuity compared to mammals due to their low number of taste buds. However, recent funding using molecular markers to label taste buds shows that birds have a well-developed gustatory system and a large number of taste buds in relation to the volume of the oral cavity.11].
Indeed, chicks (from P0 to adults) respond to chemical stimuli (e.g. hydrochloric acid, acetic acid), even at low concentrations (Soft, 1972). Although taste sensitivity cannot be quantified by behavioral responses, there is a relationship between oral response and taste sensitivity. In the future, it will be important to establish an ideal method to evaluate the actual response to chemical stimuli.
Realtime ca2+Imaging in isolated chicken taste buds has been used to investigate the response of taste cells to bitter, salty, and umami flavors and has been shown to be a functional approach to analyzing the chicken's taste senses.60]. Furthermore, a simple method recently developed for labeling chicken taste buds with molecular markers in the intact epithelial layer of the palate and floor of the oral cavity may provide an efficient way to accurately determine the number and overall distribution pattern of all taste buds. of chickens. may facilitate studies correlating taste bud volume with feeding behavior in chickens [11].
Taste quality of chickens
It is generally accepted that there are five basic taste qualities (sweet, bitter, umami, sour, salty). The various taste receptor molecules and ion channels located in the cell membrane of different types of taste bud cells are the mediating molecules that transmit various taste stimuli. Therefore, the taste receptor and ion channel gene expressions in taste bud cells are responsible for gustatory qualities. For example, taste quality in mammals is determined by taste receptor and channel gene expressions in different taste cell types, e.g. sweet by T1R2+T1R3 in type II, umami by T1R1+T1R3 in type II, bitter by T2Rs in type II, salty by ENaC in type I, sour by PCKD channels in type III cells [61].
Compared to mammals, chickens have fewer genes for taste receptors, e.g. they lack the taste receptor T1R2 for sweet [62,63] and the repertoire of bitter taste receptors is small and consists of only 3 members (T2R1, T2R2 and T2R7), in contrast to humans (25), cows (11) and mice (35) [64,65]. Unlike mammals, which have five taste qualities, chickens are believed to be able to detect only four tastes (sour, umami, salty and bitter).
Early behavioral studies have been conducted in chicks with some commonly used flavoring agents, including sucrose, saccharin, quinic acid, sodium chloride, acetic acid, and hydrochloric acid.57]. Newly hatched chicks could distinguish between bitter and sour tastes and showed aversive responses [23,57]. Bitter stimuli (e.g. quinine chloride) activate all three bitter receptors [66] for aversive reactions [57,67]. The aversive responses of chickens to quinine chloride in a dose-dependent manner are similar to those of mammals. In contrast, chickens do not show significant responses to 'sweet' stimuli, presumably due to the absence of the T1R2 receptor [23,57]. Finally, the umami taste of chicken is detected by the GPCR receptors of the T1R family (T1R1 and T1R3) [60,68,69].
In addition to the flavors described above, there are studies that indicate that chickens can also have other taste qualities. For example, chicks respond to water, while there was no significant response when using egg fluid, indicating that water alone is a strong stimulant for birds [70]. Furthermore, a recent study has shown that G protein-coupled receptor-120 mediates taste cell response to oleic acid and linoleic acid and is considered one of the functional fat taste receptors in chickens [71].
Oral responses in chicks differ from unique stimuli, and some stimuli are only perceived at certain high concentrations (fructose, sucrose, etc.) [67]. Until now, no standard method was available to determine taste responses. Different results have been reported from individual studies, which may be attributed to inconsistencies between testing methods [57,67]. Therefore, establishing a standard for studying the oral responses when exposed to unique stimuli will be important to advance our knowledge in this area.
Although chickens have unique taste bud cell types, it is unclear whether individual cell types express specific taste receptors that contribute to a specific taste. A recent report found that Gustducin+spindle-shaped cells isolated from taste buds respond to umami and bitter taste stimuli [60], corresponding to Gustducin+cells in mammals [18]. Gustducin is a G protein present in type II taste bud cells in mammals and reported to be expressed in sweet and bitter sensory taste cells in mice, hamsters, and rats.17,72,73]. However, α-Gustducin has also been identified in a large subset of chicken taste cells [20]. The expression of α-Gustducin in chicken taste cells suggests a signaling mechanism similar to that of mammals. Further research into the differentiation of individual taste cell types and the expression of different taste receptor genes specific for unique taste qualities will be essential to deepen our understanding of how taste quality is determined in chickens.
Association of taste sensitivity and quality in chickens
In chickens, taste sensitivity differs for specific taste stimuli. For example, chickens are more tolerant to 'sour' tastes compared to mammals, but they are very sensitive to 'bitter' tastes, despite having a lower number of bitter taste receptor subtypes [74], and only two of the three subtypes responsible for the bitter taste [75]. Chickens also respond strongly to umami taste stimuli consisting of inosine 5'-monophosphate and monopotassium L-glutamate, indicating that the 'umami' taste is highly conserved from birds to mammals.69]. However, they only respond to sweet and salty taste stimuli at very high concentrations (i.e. sucrose, 0-5N) [23,57].
Taste sensitivity to specific taste qualities can change under certain conditions. Zinc deficiency in chickens affects water intake and improves responses to bitter and salty taste stimuli, in stark contrast to reports in humans and rats that zinc deficiency leads to loss of taste [76,77]. Although no morphological changes in the taste buds were associated with these deficiencies, diets supplemented with these minerals caused a significant increase in responses to taste stimuli.78]. Vitamin A deficiency in chickens is also reported to cause a reduced response to taste stimuli [79], probably because vitamin A is important for maintaining the integrity of the epithelium. Similarly, vitamin A deficiency leads to a significant decrease in response to NaCl and quinine chloride stimuli in rats [80].
In summary, chickens are sensitive to gustatory cues, which is consistent with the well-developed gustatory system shown in recent studies and indicates a greater than previously thought influence on feeding behavior. The response of the birds (including chickens) to each group of taste stimuli for primary taste qualities was assessed by Roura et al. [81]. Further behavioral studies are needed for the practical applications of taste perceptions on food intake in the poultry industry.
The impact of understanding the taste experience of chicken on the poultry industry
Chickens are one of the largest animals used for egg production and meat. Taste buds are the senses that control food choices and motivate feed intake, directly impacting the productivity of these animals. In-depth knowledge of taste bud development, regulation and taste response to different stimuli helps improve feed efficiency and thus increase productivity. Further mechanistic studies on how taste bud development and taste receptor gene expression are regulated will provide information to improve feed intake and animal performance.
Recognitions
This study was supported by the National Institutes of Health (grant number R01 DC012308 to HXL) and the University of Georgia Start-up Fund to HXL.
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