Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

ACC 2024 Congress

Catch up on all the top stories and latest evidence in cardiology research with our ACC 2024 Congress hub page.
ADVANCED SEARCH
Log in
Top
Anatomical Science International
Published in: Anatomical Science International 4/2018

Open Access 01-09-2018 | Original Article

Biological aspects of the tongue morphology of wild-captive WWCPS rats: a histological, histochemical and ultrastructural study

Authors: Karolina Goździewska-Harłajczuk, Joanna Klećkowska-Nawrot, Karolina Barszcz, Krzysztof Marycz, Tomasz Nawara, Klaudia Modlińska, Rafał Stryjek

Published in: Anatomical Science International | Issue 4/2018

Login to get access

Abstract

The aim of this study was to characterise the tongue in wild-type rats using several microscopic techniques. Warsaw Wild Captive Pisula Stryjek (WWCPS) rats belong to a lineage of wild-caught rats. The study was carried out on tongues of 15 male and 15 female WWCPS rats. Histological, histochemical and ultrastructural studies were carried out. There were no significant differences between the male and female WWCPS rat tongues. There was a median groove approximately 1 cm long in the apex of the tongue that faded caudally. The intermolar prominence was clearly marked in the distal part of the lingual body. Lingual mechanical papillae located on the surface of the tongue formed four subtypes based on their shape: small filiform papillae, giant filiform papillae, thin elongated filiform papillae and wide filiform papillae. Gustatory papillae formed the second group of papillae and were divided into bud-shaped fungiform papillae, a single vallate papilla surrounded by an incomplete papillary groove and foliate papillae, which were a well-formed and composed of several pairs of folds divided by longitudinal grooves. In the posterior lingual glands (mucoserous and serous), acidic sulphated mucin-secreting cells gave a strong AB pH 2.5 positive reaction, and a positive reaction with the AB pH 1.0 stain for acidic carboxylated mucin. Double AB/PAS staining showed the presence of the majority of mucous cells with predominant of acidic mucins. Positive PAS staining showed the presence of neutral mucin. HDI staining demonstrated a weak positive reaction within Weber’s glands of the WWCPS rat tongue.
Literature
Abayomi TA, Ofusori DA, Ayoka OA, Odukoya SA, Omotoso EO, Amegor FO, Ajayi SA, Ojo GB, Oluwayinka OP (2009) A comparative histological study of the tongue of rat (Rattus norvegicus), bat (Eidolon helvum) and pangolin (Manis tricuspis). Int J Morphol 27:1111–1119CrossRef
Abumandour A, El-Bakary RMA (2013) Anatomic reference for morphological and scanning electron microscopic studies of the New Zeland white rabbits tongue (Orycotolagaus cuniculus) and their lingual adaptation for feeding habits. J Morphol Sci 30:254–265
Al-Refai AS, Omar OA, Khaial AK (2014) Effect of chamomile extract on the tongue of chemotherapy treated Albino rats (histopathological and immunohistochemical study). J Clin Cell Immunol 5:1–8
Alvarez A, Perez SI, Verzi DH (2011) Early evolutionary differentiation of morphological variation in the mandible of South American caviomorph rodents (Rodentia, Caviomorpha). J Evol Biol 24:2687–2695CrossRefPubMed
Atalar O, Karan M (2011) The light and scanning electron microscopic structure of the papilla valatae in the porcupine (Hystrix cristata). J Vet Anim Adv 10:3069–3073
Chamorro CA, de Paz P, Fernandez JG, Anel L (1993a) Fungiform papillae of the pig and the wild boar analyzed by scanning electron microscopy. Scan Microsc 7:313–322
Chamorro CA, Fernandez JG, de Paz P, Pelaze B, Anel L (1993b) Scanning electron microscopy of the wild boar and pig lingual papillae. Histol Histopathol 9:657–667
Cheng SJ, Huang CF, Chen YC, Lee JJ, Chang HH, Chen HM, Chiang ML, Kuo MY, Kok SH, Tseng CY (2009) Ultrastructural changes of posterior lingual glands after hypoglossal denervation in hamsters. J Anat 214:163–170CrossRefPubMedPubMedCentral
Ciena AP, de Sousa Bolina C, de Almeida SR, Rici RE, de Oliveira MF, de Silva MC, Miglino MA, Watanabe IS (2013) Structural and ultrastructural features of agouti tongue (Dasyprocta aguti Linnaeus, 1766). J Anat 223:152–158CrossRefPubMedPubMedCentral
Ciena AP, dos Santos AC, Vasconcelos BG, Grassi Ricci RE, de Assis Neto AC, Yomikozo de Almeida SR, Miglino MA, Watanabe I (2017) Morphological characteristics of the papillae and lingual epithelium of guinea pig (Cavia porcellus). Acta Zool. https://​doi.​org/​10.​1111/​azo.​12230 CrossRef
Costa ACBP, Pereira CA, Junqueira JC, Jorge AOC (2013) Recent mouse and rat methods for the study of experimental oral candidiasis. Virulence 4:391–399CrossRefPubMedPubMedCentral
de Abreu MA, Weckx LL, Hirata CH (2006) Histological and ultrastructural aspects of the tongue under nourished rats. Rev Bras Otorhinolaringol 72:523–527CrossRef
Doran GA, Baggett H (1971) Structural and functional classification of mammalian tongues. J Mammal 52:427–429CrossRefPubMed
Dröscher VB (1993) Białe lwy muszą umrzeć. Państwowy Instytut Wydawniczy, Warszawa
El Sharaby AA, El-Gendy SA, Alsafy MA, Nomir AG, Wakisaka S (2014) Morphological variations of the vallate papillae in some mammalian species. Anat Sci Int 89:161–170CrossRefPubMed
Elsnasharty M, El Sharaby A, Nor-El-din A (2013) Histogenessis of rabbit vallate papilla. World Acad Sci Eng Technol 76:509–516
Emura S, Tamada A, Hayakawa D, Chen H, Jamali M, Taguchi H, Shoumura S (1999a) SEM study on the dorsal lingual surface of the flying squirrel, Petaurista leucogenys. Ann Anatomy 181:495–498CrossRef
Emura S, Tamada A, Hayakawa D, Chen H, Jamali M, Ozawa Y, Shoumura S (1999b) SEM study on the dorsal lingual surface of Microtus montebelli. Okajimas Folia Anat Jpn 76:171–177CrossRefPubMed
Emura S, Tamada A, Hayakawa D, Chen H, Shoumura S (2001) SEM study of the dorsal lingual surface of the nutria, Myocastor coypus (in Japanese). Kaibogaku Zasshi 76:233–238PubMed
Emura S, Okumura T, Chen H (2011) Morphology of the lingual papillae in the Patagonian cavy. Okajimas Folia Anat Jpn 88:121–125CrossRefPubMed
Erdoğan S, Arias SV, Peréz W (2015) Morphology of the lingual surface of south American fur seal (Arctocephalus australis) and sea lion (Otaria flavescens). Microsc Res Tech 78:140–147CrossRefPubMed
Erdoğan S, Lima M, Peréz W (2016) Anatomical and scanning electron microscopic study of the tongue in the meerkat (Suricata suricatta, Shreber 1776). Anat Histol Embryol 45:51–59CrossRefPubMed
Goździewska-Harłajczuk K, Klećkowska-Nawrot J, Janeczek M, Zawadzki M (2015) Morphology of the lingual and buccal papillae in alpaca (Vicugna pacos)—light and scanning electron microscopy. Anat Histol Embrol 44:345–360CrossRef
Goździewska-Harłajczuk K, Klećkowska-Nawrot J, Nowaczyk R, Barszcz K, Przespolewska H, Kupczyńska M (2016) Biological aspect of the surface structure of the tongue in the adult red kangaroo (Macropus rufus)- light and scanning electron microscopy. Biologia 71:701–716CrossRef
Grandi D, Arcari ML, Azalli G (1994) Ultrastructural aspects of the lingual papillae in the gerbil (Meriones unguiculatus). Ital J Anat Embryol 99:201–217
Himmler BT, Stryjek R, Modlińska K, Derksen SM, Pisula W, Pellis SM (2013) How domestication modulates play behavior: a comparative analysis between wild rats and a laboratory strain of Rattus norvegicus. J Comp Psychol 127:453–464CrossRefPubMed
Hosley MA, Oakley B (1987) Postnatal development of the vallate papilla and taste buds in rats. Anat Rec 218:216–222CrossRefPubMed
Iino T, Kobayashi K (1988) Morphological studies on the lingual papillae and their connective tissue papillae of rats (in Japanese). Shigaku 75:1039–1060PubMed
Iwasaki S, Miyata K, Kobayashi K (1987) Comparative studies of the dorsal surface of the tongue in three mammalian species by scanning electron microscopy. Acta Anat 128:140–146CrossRefPubMed
Iwasaki S, Yoshizawa H, Kawahara I (1997) Study by scanning electron microscopy of the morphogenesis of three types of lingual papilla in the rat. Anat Rec 247:528–541CrossRefPubMed
Iwasaki S, Yoshizawa H, Kawahara I (1999) Ultrastructural study of the relationship between the morphogenesis of filiform papillae and the keratinization of the lingual epithelium in the rat. J Anat 195:27–38CrossRefPubMedPubMedCentral
Jackowiak H (2006) Scanning electron microscopy study of the lingual papillae in the European mole (Talpa europea L., Talpidae). Anat Histol Embryol 35:190–195CrossRefPubMed
Jackowiak H, Godynicki S (2005) The distribution and structure of the lingual papillae on the tongue of the bank vole (Clethrionomys glareolus). Folia Morphol 64:326–333
Jakob I, Hauser IA, Thevenod F, Lindemann B (1998) MDR1 in taste buds of rat vallate papilla: functional, immunohistochemical and biochemical evidence. Am J Physiol 274:C182–C191CrossRefPubMed
Jensen P (2010) Domestication, selection, behaviour and welfare of animals—genetic mechanisms for rapid responses. Anim Welfare 19:7–9
Karan M, Yilmaz S, Aydin A (2011) Morphology of the filiform lingual papillae in porcupine (Hystrix cristata). Anat Histol Embryol 40:100–103CrossRefPubMed
Kilinc M, Erdoğan S, Ketani S, Ketani MA (2010) Morphological study by scanning electron microscopy of the lingual papillae in the Middle East Blind Mole Rat (Spalax ehrenbergi, Nehring, 1898). Anat Histol Embryol 39:509–515CrossRefPubMed
Kobayashi K (1990) Three-dimensional architecture of the connective tissue core of the lingual papillae in the guinea pig. Anat Embryol 182:205–213CrossRefPubMed
Kobayashi K, Toh H, Tomo S (1992) Scanning electron microscopic study on the lingual papillae in the Manchurian chipmunk, Tamias sibiricus asiaticus. Okijamas Folia Anat Jpn 69:139–143CrossRef
Kubrakiewicz J, Jabłońska A, Mazurkiewicz-Kania M, Bilinski SM (2003) Differentiation and diversification of the follicular cells in flies: insight from the studies of the lower brachycerans’ ovaries. Genesis 36:214–224CrossRefPubMed
Kulawik M, Godynicki S (2007) Vallate papillae in the domestic rabbit (Oryctolagus cuniculus f. domestica). Pol J Vet Sci 10:47–50PubMed
Kullaa-Mikkonen A, Hynynen M, Hyvonen P (1987) Filiform papillae of human, rat and swine tongue. Acta Anat 130:280–284CrossRefPubMed
Kuru N, Çinar K, Demirbag E, Ilgun R (2017) Histological and histochemical structure of lingual salivary glands in mole rat (Spalax leucodon). Indian J Anim Res 51:252–255
Lopes JB, Watanabe IS, Soares LE, da Silva NS, da Silva MC (2009) Ultrastructural aspects of female aging Wistar rat epithelium tongue: HRSEM and TEM study. Gerontology 55:442–448CrossRefPubMed
Martinez-Vargas J, Martinez-Maza C, Munoz-Munoz F, Medarde N, Lamrous H, Lopez-Fuster MJ, Cubo J, Ventura J (2018) Comparative postnatal histomorphogenesis of the mandible in wild and laboratory mice. Ann Anat 215:8–19CrossRefPubMed
Modlińska K, Stryjek R (2016) Food neophobia in wild rats (Rattus norvegicus) inhabiting a changeable environment—a field study. PLoS ONE 11(6):e0156741CrossRefPubMedPubMedCentral
Munakata H, Isemur M, Yosizawa Z (1985) An application of the high-iron diamine staining for detection of sulfated glycoproteins (glycopeptides) in electrophoresis on cellulose acetate membrane. Tohoku J Exp Med 145:251–257CrossRefPubMed
Nagato T, Ren XZ, Toh H, Tandler B (1997) Ultrastructure of Weber’s salivary glands of the root of the tongue in the rat. Anat Rec 249:435–440CrossRefPubMed
Nonaka K, Zheng JH, Kobayashi K (2008) Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits. Okajimas Folia Anat Jpn 85:57–66CrossRefPubMed
Paliwal A, Srikantan S, De PK, Hand AR, Redman RS (2006) Histological and biochemical characterization of von Ebner’s glands in the Syrian hamster; comparison with rat von Ebner’s glands. Biotech Histochem 81:139–149CrossRefPubMed
Picoli LC, Lopes RA, Semprini M, Sala MA, Ogawa K, Watanabe T (2006) Transmission electron microscopy study of the neonatal rat tongue mucosa treated with special attention to the bacteriae on the epithelial cell membrane. Int J Morphol 24:159–163CrossRef
Prusky GT, Harker KT, Douglas RM, Whishaw IQ (2002) Variation in visual acuity within pigmented, and between pigment-ed and albino rat strains. Behav Brain Res 136:339–348CrossRefPubMed
Reginato GS, Bolina CS, Watanabe IS, Ciena AP (2014) Three-dimensional aspects of the lingual papillae and their connective tissue cores in the tongue of rats: a scanning electron microscope study. Sci World J 841879
Saber A, Weyrauch K, Salem AO (2001) Scanning electron microscopical study on the papillary body of the tongue papillae of the dromedary (Camelus dromedarius). J Cam Pract Res
Sadeghinezhad J, Tootian Z, Javadi F (2018) Anatomical and histological structure of the tongue and histochemical characteristics of the lingual salivary glands in the Persian squirrel (Sciurus anomalus). Anat Sci Int 93:58–68CrossRefPubMed
Sakr SMI, Taki-El-Deen FMA, Aboelwafa HR (2013) Comparative light and scanning electron microscopic study of the lingual papillae in three different mammalian animals: Hemiechinus auritus (Erinaceomorpha: Erinaceidae), Cavia porcellus (Rodentia: Caviidae) and Mustela nivalis vulgaris (Carnivora: Mustelidae). Life Sci J 10:3082–3093
Sachs BD (1996) Penile erection in response to remote cues from females: albino rats severely impaired relative to pigmented strains. Physiol Behav 60:803–808CrossRefPubMed
Schumacher U, Duku M, Katoh M, Jörns J, Krause WJ (2004) Histochemical similarities of mucins produced by Brunner’s glands and pyloric glands: a comparative study. Anat Rec 278:540–550CrossRef
Sheehan DC, Hrapchak BB (1980) Theory and practice histotechnology, 2nd edn. Mosby, St. Louis, MO, pp 52, 164–167
Shindo J, Yoshimura K, Kobayashi K (2006) Comparative morphological study connective on the stereo-structure of the lingual papillae and their connective tissue cores of American beaver. Okijamas Folia Anat Jpn 82:127–137CrossRef
Shumake SA, Thompson RD, Caudill CJ (1971) Taste preference behavior of laboratory versus wild Norway rats. J Comp Physiol Psychol 77:489–494CrossRefPubMed
Spicer SC, Henson JG (1967) Methods for localizing mucosubstances in epithelial and connective tissue. In: Bajusz E, Jamin F (eds) Series on methods and achievements in experimental pathology, vol 2. Karger, Basel, pp 78–112
Stangl FB, Pfau RS (1994) Gross morphology and distribution patterns of lingual papillae in some geomyid and hetromyid rodents. Proc Oklahoma Acad Sci 74:25–29
Stryjek R, Modlińska K (2016) Proces udomowienia (ulaboratoryjnienia) szczura wędrownego i jego implikacje dla badań naukowych. Kosmos 65(2):177–186
Stryjek R, Pisula W (2008) Warsaw Wild Captive Pisula Stryjek rats (WWCPS)—establishing a breeding colony of Norway rat in captivity. Pol Psychol Bull 39(2):67–70CrossRef
Stryjek R, Modlińska K, Pisula W (2012a) Species specific behavioural patterns (digging and swimming) and reaction to novel objects in wild type, Wistar, Sprague-Dawley and brown norway rats. PLoS ONE 7(7):e40642CrossRefPubMedPubMedCentral
Stryjek R, Modlińska K, Pisula W (2012b) Response to spatial and nonspatial change in wild (WWCPS) and Wistar rats. Polish Psychol Bull 43(2):124–131CrossRef
Stryjek R, Modlińska K, Turlejski K, Pisula W (2013) Circadian rhythm of outside-nest activity in wild (WWCPS), Albino and Pigmented Laboratory Rats. PLoS ONE 8(6):e66055CrossRefPubMedPubMedCentral
Tandler B, Pinkstaff CA, Riva A (1994) Ultrastructure and histochemistry of human anterior lingual salivary glands (glands of Blandin-Nuhn). Anat Rec 240:167–177CrossRefPubMed
Toprak B, Yilmaz S (2007) Investigations on postnatal development of the foliate papillae of the tongue by the light and scanning electron microscopy in the white laboratory mice. Revue Méd Vet 158:479–482
Triantafyllou A, Fletcher D, Scott J (2002) Lipolytic and esterolytic activities in posterior lingual glands of rat: a histochemical study. Histochem J 34:529–533CrossRefPubMed
Ünsaldi E (2010) Macroscopic and light microscopic structure of fungiform papillae on the tongue of squirrels (Sciurus vulgaris). Kafkas Univ Vet Fak Derg 16(1):115–118
Verli FD, Marinho SA, Rossi-Schneider TR, Yurgel LS, Lopes de Souza MA (2008) Angioarchitecture of the ventral surface of the tongue from Wistar rats. Scanning 30:414–418CrossRefPubMed
Wakisaka S, Daikoku H, Miyawaki Y, Youn SH, Maeda T, Kurisu K (1998) Immunohistochemical observation of growth-associated protein 43 (GAP-43) in the developing circumvalatte papilla of the rat. Cell Tissue Res 293:499–507CrossRefPubMed
Watanabe I, Utiyama C, Koga LY, Motoyama AA, Kobayashi K, Lopes RA, Junior BK (1997) Scanning electron microscopy study of the interface epithelium-connective tissue surface of the lingual mucosa in Calomys callosus. Ann Anat 179:45–48CrossRefPubMed
Watanabe I, Santos Haemmerle CA, Dias FJ, Cury DP, Silva MCP, Sosthines MCK, Santos TC, Guimaraes JP, Miglino MA (2013) Structural characterization of the capybara (Hydrochaeris hydrochaeris) tongue by light, scanning, and transmission electron microscopy. Microsc Res Tech 76:141–155CrossRefPubMed
Whitehead MC, Kachele DL (1994) Development of fungiform papillae, taste buds, and their innervation in the hamster. J Comp Neurol 340:515–530CrossRefPubMed
Wołczuk K (2014) Dorsal surface of the tongue of the hazel dormouse (Muscardinus avellanarius): scanning electron and light microscopic studies. Zool Pol 59:35–47CrossRef
Yoshimura K, Hama N, Shindo J, Kobayashi K, Kageyama I (2008) Light and scanning microscopic study on the lingual papillae and their connective tissue cores of the cape hyrax Procavia capensis. J Anat 213:573–582PubMedPubMedCentral
Yoshimura K, Shindo J, Kageyama I (2013) Comparative morphology of the papillae linguale and their connective tissue cores in the tongue of the greater Japanes shrew-mole, Urotrichus talpoides. Anat Histol Embryol 42:21–29CrossRefPubMed
Youn ME, Jo UB (1998) Prelectin histochemical study on glycoconjugates of rat lingual salivary glands during the postnatal development. Korean J Phys Anthropol 11:271–280CrossRef
Yücel F, Akdoğan I, Güven G, Ortuğ G (2002) SEM examination of the dorsal lingual papillae of pregnant rats. Ann Anat 184:251–255CrossRefPubMed
Metadata
Title
Biological aspects of the tongue morphology of wild-captive WWCPS rats: a histological, histochemical and ultrastructural study
Authors
Karolina Goździewska-Harłajczuk
Joanna Klećkowska-Nawrot
Karolina Barszcz
Krzysztof Marycz
Tomasz Nawara
Klaudia Modlińska
Rafał Stryjek
Publication date
01-09-2018
Publisher
Springer Singapore
Published in
Anatomical Science International / Issue 4/2018
Print ISSN: 1447-6959
Electronic ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-018-0445-y

Other articles of this Issue 4/2018

Anatomical Science International 4/2018 Go to the issue

Original Article

Anatomical relation between the accessory process and pedicle in the lumbar vertebrae

Original Article

Mash1-expressing cells could differentiate to type III cells in adult mouse taste buds

Case Report

A case of pancake kidney with a single ureter in the retroperitoneal space

Case Report

The middle rectal artery arising from the lateral sacral artery

Original Article

Clinical significance of understanding lateral and medial circumflex femoral artery origin variability

Original Article

Transmission electron microscopic and immunohistochemical observations of resting follicles of feathers in chicken show massive cell degeneration