Gustatory system neuroanatomy
These notes introduce the development of the sense of taste which can divided into five basic tastes: bitter, salty, sweet, umami (savoury) and sour. Current research appears to have displaced the historic concept of a tongue "map".
A study in rat suggests that neonatal changes in circumvallate papillae may result in postnatal changes in "taste".
In frogs, a large taste disc (TD) is the largest vertebrate gustatory organ. Postnatally, the sense of taste is also closely related to the sense of smell.
Some Recent Findings
- Nkx2-2 expressing taste cells in endoderm-derived taste papillae are committed to the type III lineage "In mammals, multiple cell-signaling pathways and transcription factors regulate development of the embryonic taste system and turnover of taste cells in the adult stage. Using single-cell RNA-Seq of mouse taste cells, we found that the homeobox-containing transcription factor Nkx2-2, a target of the Sonic Hedgehog pathway and a key regulator of the development and regeneration of multiple cell types in the body, is highly expressed in type III taste cells but not in type II or taste stem cells. Using in situ hybridization and immunostaining, we confirmed that Nkx2-2 is expressed specifically in type III taste cells in the endoderm-derived circumvallate and foliate taste papillae but not in the ectoderm-derived fungiform papillae. Lineage tracing revealed that Nkx2-2-expressing cells differentiate into type III, but not type II or type I cells in circumvallate and foliate papillae. Neonatal Nkx2-2-knockout mice did not express key type III taste cell marker genes, while the expression of type II and type I taste cell marker genes were unaffected in these mice. Our findings indicate that Nkx2-2-expressing cells are committed to the type III lineage and that Nkx2-2 may be critical for the development of type III taste cells in the posterior tongue, thus illustrating a key difference in the mechanism of type III cell lineage specification between ectoderm- and endoderm-derived taste fields."
- Taste buds are not derived from neural crest in mouse, chicken, and zebrafish "Our lineage tracing studies using multiple Cre mouse lines showed a concurrent labeling of abundant taste bud cells and the underlying connective tissue with a neural crest (NC) origin, warranting a further examination on the issue of whether there is an NC derivation of taste bud cells. In this study, we mapped NC cell lineages in three different models, Sox10-iCreERT2/tdT mouse, GFP+ neural fold transplantation to GFP- chickens, and Sox10-Cre/GFP-RFP zebrafish model. We found that in mice, Sox10-iCreERT2 specifically labels NC cell lineages with a single dose of tamoxifen at E7.5 and that the labeled cells were widely distributed in the connective tissue of the tongue. No labeled cells were found in taste buds or the surrounding epithelium in the postnatal mice. In the GFP+/GFP- chicken chimera model, GFP+ cells migrated extensively to the cranial region of chicken embryos ipsilateral to the surgery side but were absent in taste buds in the base of oral cavity and palate. In zebrafish, Sox10-Cre/GFP-RFP faithfully labeled known NC-derived tissues but did not label taste buds in lower jaw or the barbel. Our data, together with previous findings in axolotl, indicate that taste buds are not derived from neural crest cells in rodents, birds, amphibians or teleost fish."
- Review - Developing and regenerating a sense of taste "In this review, we highlight new findings in the field of taste development, including how taste buds are patterned and how taste cell fate is regulated. We discuss whether a specialized taste bud stem cell population exists and how extrinsic signals can define which cell lineages are generated. We also address the question of whether molecular regulation of taste cell renewal is analogous to that of taste bud development."
- Induction of ectopic taste buds by SHH reveals the competency and plasticity of adult lingual epithelium "Taste buds are assemblies of elongated epithelial cells, which are innervated by gustatory nerves that transmit taste information to the brain stem. Taste cells are continuously renewed throughout life via proliferation of epithelial progenitors, but the molecular regulation of this process remains unknown. During embryogenesis, sonic hedgehog (SHH) negatively regulates taste bud patterning, such that inhibition of SHH causes the formation of more and larger taste bud primordia, including in regions of the tongue normally devoid of taste buds. ... As innervation is required for SHH expression by endogenous taste buds, our data suggest that SHH can replace the need for innervation to drive the entire program of taste bud differentiation."
- Developing a sense of taste "Taste buds are found in a distributed array on the tongue surface, and are innervated by cranial nerves that convey taste information to the brain. For nearly a century, taste buds were thought to be induced by nerves late in embryonic development. However, this view has shifted dramatically. A host of studies now indicate that taste bud development is initiated and proceeds via processes that are nerve-independent, occur long before birth, and governed by cellular and molecular mechanisms intrinsic to the developing tongue. Here we review the state of our understanding of the molecular and cellular regulation of taste bud development, incorporating important new data obtained through the use of two powerful genetic systems, mouse and zebrafish."
|More recent papers
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Search term: Taste Development | Taste Embryology
- CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes "Recognition of sweet, bitter and umami tastes requires the non-vesicular release from taste bud cells of ATP, which acts as a neurotransmitter to activate afferent neural gustatory pathways. However, how ATP is released to fulfil this function is not fully understood. Here we show that calcium homeostasis modulator 1 (CALHM1), a voltage-gated ion channel, is indispensable for taste-stimuli-evoked ATP release from sweet-, bitter- and umami-sensing taste bud cells."
- FGF Signaling Regulates the Number of Posterior Taste Papillae by Controlling Progenitor Field Size "The sense of taste is fundamental to our ability to ingest nutritious substances and to detect and avoid potentially toxic ones. Sensory taste buds are housed in papillae that develop from epithelial placodes. Three distinct types of gustatory papillae reside on the rodent tongue: small fungiform papillae are found in the anterior tongue, whereas the posterior tongue contains the larger foliate papillae and a single midline circumvallate papilla (CVP). ...Here, we report that a balance between Sprouty (Spry) genes and Fgf10, which respectively antagonize and activate receptor tyrosine kinase (RTK) signaling, regulates the number of CVPs."
- Fate mapping of mammalian embryonic taste bud progenitors "Mammalian taste buds have properties of both epithelial and neuronal cells, and are thus developmentally intriguing. Taste buds differentiate at birth within epithelial appendages, termed taste papillae, which arise at mid-gestation as epithelial thickenings or placodes. ...we demonstrate that Shh-expressing embryonic taste placodes are taste bud progenitors, which give rise to at least two different adult taste cell types, but do not contribute to taste papillae. Strikingly, placodally descendant taste cells disappear early in adult life."
These are human embryonic timings, not clinical which is based on last menstral period +2 weeks GA.
Week 6 - gustatory papilla, caudal midline near the foramen caecum
Week 6-7 - nerve fibers approach the lingual epithelium
Week 8 - nerves penetrate epitheilai basal lamina and synapse with undifferentiated, elongated, epithelial cells (taste bud progenitor cell)
Week 10 - shallow grooves above the taste bud primordium
Week 12 - first differentiated epithelial cells (Type II and III)
Week 12 -13 - maximum synapses between cells and afferent nerve fibers
Week 14 - 15 - taste pores develop, mucous
Week 18 - substance P detected in dermal papillae, not in taste bud primordia
3rd Trimester -
- Links: Timeline human development
Tongue Development Parts
Oral and Pharyngeal components
Circumvallate papilla location
Tongue Week 8, (GA week 10)
Circumvallate papilla are tongue surface specialisation of large size, varying in number (8-12) forming an inverted letter V shape on the dorsum of the tongue immediately in front of the foramen cecum and sulcus terminals. Numerous "taste buds" are located on the sides of these circumvallate papilla (vallate papilla)as well as with fungiform papilla. The three types of tongue papillae from numerous to few are: filiform, fungiform and circumvallate.
Other adult locations include the fimbriæ linguæ, under surface of the soft palate, and on the posterior surface of the epiglottis.
- Links: Histology HE | Histology VG | Drawing - circumvallate papillae | Tongue Development
Gustatory Cranial Sensory Neurons
Cranial nerves VII, IX and X have dual embryonic origins and provide both gustatory (taste) and non-gustatory (touch, pain, temperature) sensory innervation to the oral cavity of vertebrates.
- originate from epibranchial placodes
- innervate taste buds
- project centrally to the rostral nucleus of the solitary tract (NTS)
General Epithelial Innervation of the oral cavity
- originate from cranial neural crest
- innervation to the oropharynx
- project to non-gustatory hindbrain regions (spinal trigeminal nucleus)
(text based on: Embryonic origin of gustatory cranial sensory neurons.)
Section (B4) through head showing tongue and head structures.
|Mouse Tongue Pax9 Expression in Different Taste Papillae
||E13.5 Mouse Tongue Pax9 Expression in Different Taste Papillae
- A. Drawing showing the localization of the circumvallate papilla (CVP), foliate papillae (FOP), and fungiform papillae (FUP) in the mouse tongue.
- B. Whole mount X-Gal staining of a Pax9+/LacZ mouse tongue at embryonic day 13.5 (E13.5).
Note that expression is also seen in the mesenchyme adjacent to the developing FOP (arrowheads) and that the color reaction was stopped before epithelial staining began to obscure the mesenchymal expression domain.
B Scale bar 200 µm.
||E13.5 -E18.5 Mouse Tongue Pax9 Expression in Different Taste Papillae
Pax9 immunostaining of taste papillae during development on cross sections (C–F; K–N) and horizontal sections of the tongue (G–J).
- C–F Pax9 is expressed in the epithelium during CVP morphogenesis and is down-regulated in some regions of the trenches at E18.5 (arrowhead in F).
- G–J In addition to the epithelium, Pax9 is also expressed in the mesenchyme during FOP development, while reduced Pax9 levels were observed in the trenches at E18.5 (arrowhead in J).
- K–N In the anterior part of the tongue Pax9 is expressed in the FUP epithelium and in filiform papillae (FIP). Note that the expression is very weak or absent in the taste placodes (arrowheads).
Scale bars 50 µm.
Images and data.
- Links: mouse | PAX
- ↑ Chandrashekar J, Hoon MA, Ryba NJ & Zuker CS. (2006). The receptors and cells for mammalian taste. Nature , 444, 288-94. PMID: 17108952 DOI.
- ↑ Krimm RF. (2007). Factors that regulate embryonic gustatory development. BMC Neurosci , 8 Suppl 3, S4. PMID: 17903280 DOI.
- ↑ Sbarbati A, Crescimanno C, Merigo F, Benati D, Bernardi P, Bertini M & Osculati F. (2001). A brief survey of the modifications in sensory-secretory organs of the neonatal rat tongue. Biol. Neonate , 80, 1-6. PMID: 11474141 DOI.
- ↑ Qin Y, Sukumaran SK & Margolskee RF. (2021). Nkx2-2 expressing taste cells in endoderm-derived taste papillae are committed to the type III lineage. Dev Biol , 477, 232-240. PMID: 34097879 DOI.
- ↑ Yu W, Wang Z, Marshall B, Yoshida Y, Patel R, Cui X, Ball R, Yin L, Kawabata F, Tabata S, Chen W, Kelsh RN, Lauderdale JD & Liu HX. (2021). Taste buds are not derived from neural crest in mouse, chicken, and zebrafish. Dev Biol , 471, 76-88. PMID: 33326797 DOI.
- ↑ Barlow LA & Klein OD. (2015). Developing and regenerating a sense of taste. Curr. Top. Dev. Biol. , 111, 401-19. PMID: 25662267 DOI.
- ↑ Castillo D, Seidel K, Salcedo E, Ahn C, de Sauvage FJ, Klein OD & Barlow LA. (2014). Induction of ectopic taste buds by SHH reveals the competency and plasticity of adult lingual epithelium. Development , 141, 2993-3002. PMID: 24993944 DOI.
- ↑ Kapsimali M & Barlow LA. (2013). Developing a sense of taste. Semin. Cell Dev. Biol. , 24, 200-9. PMID: 23182899 DOI.
- ↑ Taruno A, Vingtdeux V, Ohmoto M, Ma Z, Dvoryanchikov G, Li A, Adrien L, Zhao H, Leung S, Abernethy M, Koppel J, Davies P, Civan MM, Chaudhari N, Matsumoto I, Hellekant G, Tordoff MG, Marambaud P & Foskett JK. (2013). CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature , 495, 223-6. PMID: 23467090 DOI.
- ↑ Petersen CI, Jheon AH, Mostowfi P, Charles C, Ching S, Thirumangalathu S, Barlow LA & Klein OD. (2011). FGF signaling regulates the number of posterior taste papillae by controlling progenitor field size. PLoS Genet. , 7, e1002098. PMID: 21655085 DOI.
- ↑ Thirumangalathu S, Harlow DE, Driskell AL, Krimm RF & Barlow LA. (2009). Fate mapping of mammalian embryonic taste bud progenitors. Development , 136, 1519-28. PMID: 19363153 DOI.
- ↑ Witt M & Reutter K. (1996). Embryonic and early fetal development of human taste buds: a transmission electron microscopical study. Anat. Rec. , 246, 507-23. PMID: 8955790 <507::AID-AR10>3.0.CO;2-S DOI.
- ↑ Harlow DE & Barlow LA. (2007). Embryonic origin of gustatory cranial sensory neurons. Dev. Biol. , 310, 317-28. PMID: 17826760 DOI.
- ↑ Kist R, Watson M, Crosier M, Robinson M, Fuchs J, Reichelt J & Peters H. (2014). The formation of endoderm-derived taste sensory organs requires a Pax9-dependent expansion of embryonic taste bud progenitor cells. PLoS Genet. , 10, e1004709. PMID: 25299669 DOI.
Nehring I, Kostka T, von Kries R & Rehfuess EA. (2015). Impacts of in utero and early infant taste experiences on later taste acceptance: a systematic review. J. Nutr. , 145, 1271-9. PMID: 25878207 DOI.
Domínguez PR. (2011). The study of postnatal and later development of the taste and olfactory systems using the human brain mapping approach: an update. Brain Res. Bull. , 84, 118-24. PMID: 21184814 DOI.
Niki M, Yoshida R, Takai S & Ninomiya Y. (2010). Gustatory signaling in the periphery: detection, transmission, and modulation of taste information. Biol. Pharm. Bull. , 33, 1772-7. PMID: 21048297
Chaudhari N & Roper SD. (2010). The cell biology of taste. J. Cell Biol. , 190, 285-96. PMID: 20696704 DOI.
Beauchamp GK & Cowart BJ. (1985). Congenital and experiential factors in the development of human flavor preferences. Appetite , 6, 357-72. PMID: 3911888
Schwartz C, Issanchou S & Nicklaus S. (2009). Developmental changes in the acceptance of the five basic tastes in the first year of life. Br. J. Nutr. , 102, 1375-85. PMID: 19505346 DOI.
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Torrey TW. The influence of nerve fibers upon taste buds during embryonic development. (1940) Proc Natl Acad Sci U S A. 26(11):627-34. PMID 16577985
Mouse circumvallate papilla
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Cite this page: Hill, M.A. (2023, December 2) Embryology Sensory - Taste Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Sensory_-_Taste_Development
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