Okajimas Folia Anat. Jpn., 56(5) : 309-316, December 1979 Morphology of the Tongue Muscles of the Mouse with Special Reference to the Genioglossus Muscle By IKUO YOSHIOKA, MICHIKO IIDA and HIROSHI MUTO Department of Anatomy, Aichi Medical University, Nagakute, Aichi 480-11, Japan Received for Publication, May 21, 1978 Key Words: Tongue muscles, Genioglossus muscle, Mouse. Summary. The mouse tongue musculature and its movements were studied macroscopically. The attachment of the extrinsic tongue muscles was also ascertained by dissection and light microscopy. 1. The genioglossus muscle of the mouse was attached to the posterior surface of the midsagittal region of the mandibular symphysis but medial and posterior to the geniohyoid tendon. 2. The genioglossus muscle was divided into three parts. Its anterior border was not straight and did not coincide with that of the intermolar eminence. This means that as in animals without an intermolar eminence, the anterior border of the genioglossus does not always coincide with an intermolar eminence. 3. On closing or opening of the mouth, the tongue shape changed in the dorsum linguae, showing an intimate relationship with the genioglossus muscle, but the position of the geniohyoid muscle remained almost static. Introduction It has been shown in many morphological, radiographic and electromyographic investigations that the extrinsic tongue muscles are intimately related to tongue protrusion and retraction. Valuable contributions to our understanding of the structure and function of the tongue musculature in the cat and man were made by Abd-el-Malek (1938, 1939, 1955). Livingston (1956) discussed three aspects of the movement of the tongue based on morphological studies of tongues from various animals : (1) tongue movements are probably due to movement of the hyoid bone ; (2) tongue mobility may be considered as a change in position cornbined with a change of form, being due to extrinsic muscles ; (3) the mobility of the tongue derives from its intrinsic musculature. Doran and Baggett (1971) classified mammalian tongues into two types on the basis of their structural and functional characteristics. Further, in several mammalian tongues, they (1972) described the structure of the genioglossus muscle and its relationship to tongue function. Radiographic studies of the rabbit and human tongue during swallowing have indicated that apposition of this area of the tongue to the palate occurred (Ardran and Kemp, 1955 ; Ardran et al., 1958). Electrographic 309
310 1. Yoshioka, M. lida and H. - Muto studies of the extrinsic muscles of the human tongue revealed that its main actions such as protrusion, retraction and modification of the tongue shape could be correlated with the electromyographic activity of each muscle (Sauerland and Mitchell, 1975). It has also been reported that each muscle indicated a general pattern of muscular activity during swallowing, and each individual had his own swallowing pattern (Cunningham and Basmajian, 1969, 1972). In spite of the above investigations, the relationship between the extrinsic musculature and function of the tongue has been ignored. The present paper therefore describes certain findings on the topographical anatomy and function of the exrinsic musculature of the mouse tongue. Materials and Methods Nine female adult SMA mice (20.5-32.0 g) were used in the present study. They were sacrificed by chloroform anesthesia and their heads were removed and fixed in 10% formalin solution with the mouth in a closing or (*ening state of various grades. After each head had been sectioned in the mid-sagittal plane, this plane was observed under a dissecting microscope. In addition, 2 male (30.5 and 37.8 g) and 3 other female adult SMA mice (21.0-31.5 g) were sacrificed by chloroform anesthesia, and their tongues with the mandibles were fixed in 10% formalin solution. The mandibles were then decalcified with 6% nitric acid. The materials were dehydrated in a graded ethanol series, embedded in paraffin and serially cut at 6 to 10,tim in sagittal or horizontal sections. The sections obtained were stained with hematoxylineosin. Results 1. Tongue musculature In the superficial layer of the tongue, superficial longitudinal fibers were found to run in a longitudinal direction throughout the entire dorsal surface of the Fig. 1. Diagram of the extrinsic tongue muscles of the mouse. A, B and C: three parts of genioglossus, GH : geniohyoid, 1E: intermolar eminence.
Morphology of the Tongue Muscles of the Mouse 311 tongue. Also, in the superficial layer of the inferior surface of the tongue, deep longitudinal fibers ran in a longitudinal direction from the anterior edge of the intermolar eminence to the tongue tip. The transverse and vertical muscles formed a core in the tongue crossing one another at right angles. The genioglossus muscle was attached inferiorly to the mid-sagittal region of the mandibular symphysis but medially and superiorly to the geniohyoid tendon. The extent of this muscle was confined to between the rear of the anterior tongue and a vallate papilla, but the fibers did not reach to the tongue tip. It did not have a straight anterior border and was divided into 3 parts : an anterior part running to the posterior half of the anterior tongue, a middle part between the anterior border of the intermolar eminence and the vallate papilla, and a posterior part extending to the tongue root (Fig. 1). 2. Changes of tongue shape In the mouth in the closed state, the dorsal surface of the tongue was on the highest level in the intermolar eminence and gradually became lower anteriorly and posteriorly (Fig. 2). In the midsagittal plane, the genioglossus extended towards the dorsal surface of the tongue in a fan-shaped configuration, with its anterior part extending to the porterior half of the anterior tongue, the middle part to the intermolar eminence and the posterior part to the tongue root. In the closed state, the dorsal surface of the tongue touched the hard palate except in very narrow spaces between the tongue and palatal transverse furrows. In the posterior region of the mouth, there was a narrow space between the tongue root and soft palate. In the slightly or moderately opening mouth, the part just anterior to the intermolar eminence was depressed by traction of the anterior part of the genioglossus with descent of the mandibular junctional part. At the same time, the tongue root was also depressed in relation to the posterior part of the genioglossus. As a result of the depression in these parts, the intermolar emince protruded distinctly. Thus, only the intermolar eminence touched the hard and soft palates, and the anterior tongue was apart from the palate (Figs. 3, 4). The position of the hyoid bone was almost static in the opening mouth as compared to that in the closed state of the mouth. Discussion The musculature of the tongue is intimately related to tongue modification and swallowing. Livingston (1956) suggested that tongue movements were probably due to movements of the hyoid bone since in its simplest from, the tongue consists of a process of the hyoid apparatus, the entoglossal process, covered with a mucous membrane, and the tongue of higher mammals is associated with the hyoid bone and can be moved by virtue of this association, involving the muscles of the floor of the mouth, the suprahyoid muscles. Livingston also stated that tongue mobility might be combined with changes of form and this was due to extrinsic muscles such as the hyoglossus, styloglossus and genioglossus. In the present study, the genioglossi were found to be transformed with mobility of the mouth, but the position of the hyoid bone remained almost static. It is considered therefore that in the tongue movements, the genioglossus was of greatest importance among all the tongue muscles, and movements of the geniohyoid and hyoid bone were related rather to swallowing
312 I. Yoshioka, M. Lida and 11 Muto than tongue movements during mastication. Regarding tongue mobility, Doran and Baggett (1972) reported in the wallaby, rat, guinea-pig, sheep and human tongue that the genioglossus muscle was divided structurally and functionally into 2 or 3 parts, each with separate attachments and an intimate relationship to the' geniohyoid muscles, and that the anterior border of the genioglossus was related to that of the intermolar eminence in animals where the latter was present. Based on these findings, they concluded that the combined action of the genioglossus was to protrude and depress the tongue and not to retract the tongue tip, as is often stated. In the mouse tongue, although the anterior fibers of the genioglossus did not extend to the tongue tip, its anterior border was not straight as in their description, but reached to the middle part of the anterior tongue in front of the anterior border of the intermolar eminence. The mouse tongue can be divided into 4 parts based on the distribution of bundles and fibers in the genioglossus muscle : the part near the tongue tip excluding the genioglossus fibers (I), the posterior half of the anterior tongue related to its anterior bundle (II), the posterior tongue corresponding to the intermolar eminence to the middle bundle (III) and the tongue root to the posterior bundle (IV). It was also noted in the present experiments that the genioglossus was related to protrusion and depression of the dorsal surface of the tongue. Only with movement of the mouth, was the tongue surface protruded or depressed by each attachment of the genioglossus bundles being tense or flaccid. In the closed mouth, the space between the tongue and hard palate was extremely narrow like that between the tongue root and soft palate, while in the opening mouth,' a small space appeared in the anterior part of the oral cavity. However, the change in posterior space with movement of the mouth was not remarkable. In Fig. 3, the posterior space is apparently rather narrow be cause of descent of the soft palate in spite of depression of part IV and protrusion of part III. Abd-el-Malek (1938, 1939) studied the tongue musculature of the cat and man, and noted that most of the anterior fibers of the genioglossus reached directly into the tongue tip. Some authors have therefore considered that these fibers can retract the tongue tip (Abd-el-Malek, 1955 ; Cunningham, 1964 ; Gardner, 1969). In contrast, Doran and Baggett (1972) reported that in the midsagittal plane of the wallaby, rat, guinea-pig, sheep and human tongue, none of the genioglossus fibers reached into the tongue tip, and they concluded that the genioglossus did not retract the tip. In the present study also, the genioglossus did not reach to the tongue tip as described by Doran and Baggett. However, because its anterior fibers were distributed in the posterior half of the anterior tongue (II), without relation to the anterior border of the intermolar eminence, it seems likely that this muscle can retract the tongue tip (I). Doran and Baggett (1972) further noted. that the anterior border of the genioglossus of animals coincided with that of the intermolar eminence, and suggested that in animals without an intermolar eminence, the area bounded by the genioglossus might therefore act as an intermolar eminence during mastication. However, in the present study, the anterior border of the genioglossus did not coincide with that of the of the intermolar eminence, but passed to the area forward of the intermolar eminence.
Morphology of the Tongue Muscles of the Mouse 313 This means that as in animals without an intermolar eminence, the anterior border of the genioglossus does not always coincide with an intermolar eminence. On the intermolar eminence of the mouse, the filiform papillae are larger than in other areas of the tongue; they form the giant conical papillae named by Kutuzov and Sicher (1953). In a cineradiographic study of rabbit tongue movements, apposition of the intermolar eminence to the palate was found to occur during swallowing (Ardran et al., 1955). The present study indicates that bunching of this area against the palate is effected by contraction of the anterior and posterior parts of the genioglossus, although the experiment could not explain the role of the geniohyoid during swallowing. Doran and Baggett stated that the attachment of the anterior fibers of the genioglossus was lateral to the geniohyoid tendon in the animals which they examined. In contrast, we observed in macroscopic specimens and serial sections of the mouse tongue, that the attachment of the geniolossus tendon was on the posterior surface of the mandibular junction, adjacent upwards medially to the geniohyoid tendon. References 1) Abd-el-Malek, S.: A contribution to the study of the movements of the tongue in animals, with special reference to the cat. J. Anat., 78: 15-30, 1938. 2) Abd-el-Malek, S.: Observations on the morphology of the human tongue. ibid., 13: 201-210, 1939. 3) Abd-el-Malek, S.: The part played by the tongue in mastication and deglutition. ibid., 89: 250-254, 1955. 4) Ardran, G.M. and Kemp, F.H.: A radiographic study of movements of the tongue in swallowing. Dent. Pract., 8: 252-261, 1955. 5) Ardran, G.M., Kemp, F.H. and Ride, W.D.L. : Radiographic analysis of mastication and swallowing in the domestic rabbit : Oryctolagus criniculus. Proc. Zool. Soc. London, 130: 257-274, 1958. 6) Cunningham, D.J. : Cunningham's textbook of anatomy, 10th ed. (Romanes, G.J. ed.), 289-290. Oxford Univ. Press, London, 1964. 7) Cunningham, D.P. and Basmajian, J.V.: Electromyography of genioglossus and geniohyoid muscles during deglutition. Anat. Rec., 165: 401-410, 1969. 8) Doran, G.A. and Baggett, H.: A structural and functional classification of mammalian tongues. J. Mamm., 52 : 427-429, 1971. 9) Doran, G.A. and Baggett, H.: The genioglossus muscle : A reassement of its anatomy in some mammals, including man. Acta Anat., 83: 403-410, 1972. 10) Gray, H.: Gray's anatomy, 13th ed. (Davies, D.V. and Coupland, R.E. ed.), 1427-1428. Longmans, London, 1967. 11) Hrycyshyn, A.W. and Basmajian, J.V.: Electromyography of the oral stage of swallowing in man. Am. J. Anat., 133: 333-340, 1972. 12) Livingston, R.M. : Some observations on the natural history of the tongue. Ann. Roy. Coll. Surg. England, 19: 185-200, 1956. 13) Sauerland, E.K. and Mitchell, S.P. : Electromyographic activity of intrinsic and extrinsic muscles of the human tongue. Texas Rep. Biol. Med., 33 : 445-455, 1957.
314 I. Yoshioka, M. lida and H. Muto Explanation of Figures Plate I Fig. 2. Mid-sagittal plane of mouse tongue in the state of the closed mouth. Fig. 3. The same region in the state of the slightly opening mouth. Fig. 4. The same region in the state of the moderately opening mouth.
315 Plate I I. Yoshioka, M. Iida and H. Muto