Microanatomy and Spatial Distribution of the Tongue Musculature of the Lesser Bamboo Rat (Cannomys badius)
Keywords:
muscular hydrostat, rodent, tongue movement, tongue muscles, 3D reconstructionAbstract
The mammalian tongue consists of complex arrays of intertwining muscle fibers, the functions of which are based upon hydrostatic deformation and are directly responsible for food processing. The anatomy of tongue musculature has been well-described in the laboratory rat and mouse, representative of other rodents, but is lacking in wild species. Accordingly, this study presents a detailed description of the muscular structures of the lesser bamboo rat’s tongue, a wild rodent distributed in Indochina. Primarily, serial coronal sections of three tongues were taken, stained, and histologically examined. The outlines and configurations of tongue muscles were observed and then used to construct three-dimensional (3D) visuals that facilitated evaluation of the interrelated anatomical orientation of muscles. Sagittal sections in one specimen reinforced the 3D depiction by providing details of the intricate myoarchitecture along the entire tongue length. As by-products of serial sectioning, the distributions of the lingual artery and the hypoglossal nerve were also traced at the posterior part of the tongue. The overall anatomy of the lesser bamboo rat’s tongue is similar to that of the rat and mouse, but two principal noticeable differences among the three rodents were found in the anterior tongue: (i) the arrangement of the transversus muscle pertaining to longitudinal muscles and (ii) the end point of the genioglossus muscle. These orientations may be associated with movements of the tongue tip. Based on the anatomy of the tongue musculature in conjunction with its arterial and nerve supplies, types of tongue movements in the lesser bamboo rat are also proposed and explained in relation to food manipulation; enlightening the structure-function relationships for this complex muscle organ.
References
Abe, S., Maejima, M., Watanabe, H., Shibahara, T., Agematsu, H., Doi, T., Sakiyama, K., Usami, A., Gojyo, K., Hashimoto, M., Yoshinari, M. and Ide, Y. 2002. Muscle-fiber characteristics in adult mouse-tongue muscles. Anatomical Science International, 77: 145–148.
Aldes, L.D. 1995. Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat. Journal of Comparative Neurology, 353: 89–108.
Aoyagi, H., Iwasaki, S.I. and Nakamura, K. 2015. Three-dimensional observation of mouse tongue muscles using micro-computed tomography. Odontology, 103: 1–8.
Ciena, A.P., Bolina, C.S., Almeida, S.R., Rici, R.E.G., Oliveira, M.F., Silva, M.C.P., Miglino, M.A. and Watanabe, I. 2013. Structural and ultrastructural features of the agouti tongue (Dasyprocta aguti Linnaeus, 1766). Journal of Anatomy, 223: 152–158.
Cizek, P., Hamouzova, P., Goździewska-Harłajczuk, K., Klećkowska-Nawrot, J. and Kvapil, P. 2020. Microscopic structure of the tongue in the lesser hedgehog tenrec (Echinops telfairi, Afrosoricida) and its relation to phylogenesis. Anatomical Science International, 95: 313–322.
Dinç, G., Yilmaz, S., Karan, M., Aydin, A. and Atalar, Ö. 2010. Study by light and scanning electron microscopy of the fungiform papillae on tongue of the porcupine (Hystrix cristata). Firat University Veterinary Journal of Health Sciences, 24: 99–102.
Dobbins, E.G. and Feldman, J.L. 1995. Differential innervation of protruder and retractor muscles of the tongue in rat. Journal of Comparative Neurology, 357: 376–394
Doran, G.A. 1975. Review of the evolution and phylogeny of the mammalian tongue. Acta Anatomica, 91: 118–129.
Doran, G.A. and Baggett, H. 1971. A Structural and Functional Classification of Mammalian Tongues. Journal of Mammalogy, 52: 427–429.
Doran, G.A. and Baggett, H. 1972. The genioglossus muscle: a reassessment of its anatomy in some mammals, including man. Acta Anatomica, 83: 403–410.
El-Bakary, N.E.R. and Abumandour, M.M.A. 2017. Morphological studies of the tongue of the Egyptian water buffalo (Bubalus bubalis) and their lingual papillae adaptation for its feeding habits. Anatomia Histologia. Embryologia, 46: 474–486.
Erdoğan, S., Lima, M. and Pérez, W. 2016. Anatomical and scanning electron microscopic study of the tongue in the meerkat (Suricata suricatta, Schreber, 1776). Anatomia Histologia. Embryologia, 45: 51–59.
Fogarty, M.J. and Sieck, G.C. 2021. Tongue muscle contractile, fatigue, and fiber type properties in rats. Journal of Applied Physiology, 131: 1043–1055.
Fucci, D. and Petrosino, L. 1981. The human tongue: normal structure and function and associated pathologies. Speech and Language, 6: 305–374.
Gilbert, R.J., Napadow, V.J., Gaige, T.A. and Wedeen, V.J. 2007. Anatomical basis of lingual hydrostatic deformation. Journal of Experimental Biology, 210: 4069–4082.
Goździewska-Harlajcuk, K., Klećkowska-Nawrot, J., Barszcz, K., Marycz, K., Nawara, T., Modliǹska, K. and Stryjek, R. 2018. Biological aspects of the tongue morphology of wild-captive WWCPS rats: A histological, histochemical and ultrastructural study. Anatomical Science International, 93: 514–532.
Hammer, Ø., Harper, D.A.T. and Ryan, P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4: 1–9.
Hellekant, G., 1972. Circulation of the tongue. In: Emmelin, M. and Zotterman, Y. (Eds). Oral Physiology: Proceedings of the International Symposium Held in Wenner-Gren Center, Stockholm. Pergamon Press Ltd., Oxford, pp. 127–138.
Hellstrand, E. 1980. Morphological and histochemical properties of tongue muscles in cat. Acta Physiologica Scandinavica, 110: 187–198.
Hellstrand, E., 1981. Contraction times of the cat's tongue muscles measured by light reflection. Innervation of individual tongue muscles. Acta Physiologica Scandinavica, 111: 417–423.
Igbokwe, C.O. and Mbajiorgu, F.E. 2019. Anatomical and scanning electron microscopic study of the tongue in the African giant pouched rats (Cricetomys gambianus, Waterhouse). Anatomia Histologia. Embryologia, 48: 455–465.
Isarankura Na Ayudhya, J. and Wannaprasert, T. 2020. Tooth morphology and enamel microstructure of the lesser bamboo rat (Cannomys badius). Mammal Study, 45: 219–228.
Jackowiak, H. and Godynicki, S. 2005. The distribution and structure of the lingual papillae on the tongue of the bank vole Clethrinomys glareolus. Folia Morphologica, 64: 326–333.
John, J., Bailey, E.F. and Fregosi, R.F. 2005. Respiratory-related discharge of genioglossus muscle motor units. American Journal of Respiratory and Critical Care Medicine, 172: 1331–1337.
Kayalioglu, M., Shcherbatyy, V., Seifi, A. and Liu, Z.J. 2007. Roles of intrinsic and extrinsic tongue muscles in feeding: Electromyographic study in pigs. Archives of Oral Biology, 52, 786–796.
Kidder, I.J., Mudery, J.A. and Bailey, E.F. 2014. Neural drive to respiratory muscles in the spontaneously breathing rat pup. Respiratory Physiology & Neurobiology, 202: 64–70.
Kier, W.M. and Smith, K.K. 1985. Tongues, tentacles and trunks: the biomechanics of movement in muscular-hydrostats. Zoological Journal of the Linnean Society, 83: 307–324.
Kilinc, M., Erdogan, S., Ketani, S. and Ketani, M.A. 2010. Morphological study by scanning electron microscopy of the lingual papillae in the Middle East blind mole rat (Spalax ehrenbergi, Nehring, 1898). Anatomia Histologia. Embryologia, 39: 509–515.
Lekagul, B. and McNeely, J.A. 1988. Mammal of Thailand, second ed. Darnsutha Press, Bangkok, 758 pp.
Maejima, M., Abe, S., Sakiyama, K., Agematsu, H., Hashimoto, M., Tamatsu, Y. and Ide, Y. 2005. Changes in the properties of mouse tongue muscle fibres before and after weaning. Archives of Oral Biology, 50: 988–993.
McClung, J.R. and Goldberg, S.J. 1999. Organization of motoneurons in the dorsal hypoglossal nucleus that innervate the retrusor muscles of the tongue in the rat. Anatomical Record, 254: 222–230.
McClung, J.R. and Goldberg, S.J. 2000. Functional anatomy of the hypoglossal innervated muscles of the rat tongue: A model for elongation and protrusion of the mammalian tongue. Anatomical Record, 260: 378–386.
Mu, L. and Sanders, I. 1999. Neuromuscular organization of the canine tongue. Anatomical Record, 256: 412–424.
Mu, L. and Sanders, I. 2000. Neuromuscular specializations of the pharyngeal dilator muscles: II. Compartmentalization of the canine genioglossus muscle. Anatomical Record, 260: 308–325.
Mu, L. and Sanders, I. 2010. Human tongue neuroanatomy: Nerve supply and motor endplates. Clinical Anatomy, 23: 777–791.
Nakajima, T., Hanai, H., Asano, T. and Yasuda, K. 1982. Arterial distribution in the floor region of the rabbit mouth using the plastic injection method. Okajimas Folia Anatomica Japonica, 58: 235–246.
Naksatit, N. and Rojanadilok, P. 1988. The underground world of the bamboo rat. Feature Magazine, 4: 56–69.
Napadow, V.J., Chen, Q., Wedeen, V.J. and Gilbert, R.J. 1999. Biomechanical basis for lingual muscular deformation during swallowing. American Journal of Physiology-Gastrointestinal and Liver Physiology, 277: G695–G701.
Nonaka, K., Zheng, J.H. and Kobayashi, K. 2008. Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits. Okajimas Folia Anatomica Japonica, 85: 57–66.
Norris, R.W. 2017. Family Spalacidae (muroid mole‐rats). In: Wilson, D.E., Jr Lacher, T.E. and Mittermeier, R.A. (Eds). Handbook of the Mammals of the World. Vol. 7. Rodents II. Lynx Edicions, Barcelona, pp. 108–142.
O'Reilly, P.M. and FitzGerald, M.J. 1990. Fibre composition of the hypoglossal nerve in the rat. Journal of Anatomy, 172: 227–243.
Sadeghinezhad, J., Tootian, Z. and Javadi, F. 2018. Anatomical and histological structure of the tongue and histochemical characteristics of the lingual salivary glands in the Persian squirrel (Sciurus anomalus). Anatomical Science International, 93: 58–68.
Sanders, I. and Mu, L. 2013. A three-dimensional atlas of human tongue muscles. Anatomical Record, 296: 1102–1114.
Shimizu, T., 1986. The lingual artery of the rat. Okajimas Folia Anatomica Japonica, 63: 47–66.
Smith, K.K., 1989. Histological demonstration of muscle spindles in the tongue of the rat. Archives of Oral Biology, 34: 529–534.
Stavness, I., Lloyd, J.E. and Fels, S. 2012. Automatic prediction of tongue muscle activations using a finite element model. Journal of Biomechanics, 45: 2841–2848.
Sutlive, T.G., Shall, M.S., McClung, J.R. and Goldberg, S.J., 2000. Contractile properties of the tongue's genioglossus muscle and motor units in the rat. Muscle & Nerve, 23: 416–425.
Takemoto, H., 2001. Morphological analyses of the human tongue musculature for three-dimensional modeling. Journal of Speech, Language, and Hearing Research, 44: 95–107.
Takemoto, H., 2008. Morphological analyses and 3D modeling of the tongue musculature of the chimpanzee (Pan troglodytes). American Journal of Primatology, 70: 966–975.
Wannaprasert, T., Phanthuma-opas, P. and Jindatip, D. 2020. Morphology and microstructure of the tongue of the lesser bamboo rat (Cannomys badius). Acta Zoologica, 101: 282–291.
Wedeen, V.J., Reese, T.G., Napadow, V.J. and Gilbert, R.J. 2001. Demonstration of primary and secondary muscle fiber architecture of the bovine tongue by diffusion tensor magnetic resonance imaging. Biophysical Journal, 80: 1024–1028.
Yoshioka, I., Iida, M. and Muto, H. 1979. Morphology of the tongue muscles of the mouse with special reference to the genioglossus muscle. Okajimas Folia Anatomica Japonica, 56: 309–316.
Zaidi, F.N., Meadows, P., Jacobowitz, O. and Davidson, T.M. 2013. Tongue anatomy and physiology, the scientific basis for a novel targeted neurostimulation system designed for the treatment of obstructive sleep apnea. Neuromodulation: Technology at the Neural Interface. 16: 376–386.
Downloads
Published
How to Cite
Issue
Section
Categories
License
Chulalongkorn University. All rights reserved. No part of this publication may be reproduced, translated, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without prior written permission of the publisher
