JOURNAL OF MORPHOLOGY 204139-146 (1990)
Videofluorographic Analysis of Tongue Movement in the Rabbit (Oryctolaguscuniculus) DAVID CORTOPASSI AND ZANE F. MUHL Department of Orthodontics, University of Illinois at Chicago, Chicago, Illinois 60612
ABSTRACT The movement of the entire tongue and intermolar eminence during mastication is described in the domestic rabbit (Oryctolagus cuniculus). Tongue movement and jaw position were analyzed videofluorographically from separate lateral and dorso-ventralviews in six rabbits. Metallic markers were inserted into the tongue so that its movement was visible on the fluorographicimage. Frame-by-frame analysis of the videofluorographictape recordings demonstrates that tongue movement in all animals was identical in direction during each part of the chewing cycle. In the lateral view the forepart of the tongue moves down and forward during the opening stroke, whereas the intermolar eminence moves up and forward to appose the palate. During the closing stroke, as the tip of the tongue moves up and back, the intermolar eminence lowersfrom the palate and retracts. During the power stroke the forepart of the tongue is at its most elevated and retruded position, while the intermolar eminence is its lowest and most retruded. The dorso-ventralview showed that lateral movement of the tongue and mandible are highly synchronous. The intermolar eminence decreases in width during the power stroke, possibly twisting to place or keep food on the teeth. An anterior to posterior undulating movement of the entire tongue occurs throughout the chewing cycle. As the intermolar eminence elevates to appose the palate during the opening stroke, it may replace the bolus on the teeth on the chewing side. The intermolar eminence also appears to be twisting during the closing and power strokes to place or maintain food on the teeth. In recent years mastication has been studied in many mammalian species,focusing mainly on the morphology of the jaws and teeth and their function in food breakdown. The function of the tongue in intraoral food transport during mastication has also been described in some mammals, e.g., for rabbits (Ardran et al., '58), bats (de Gueldre and de Vree, 'M), opossums (Hiiemae and Crompton, '71),rats (Weijs,'75), cats (Thexton, '80), macaques (Franks et al., '84)' and the hyrax (Franks et al., '85). The intermolar eminence is an elevation located on the dorsal surface of the tongue between the cheek teeth of some herbivorous ungulates, lagomorphs, and rodents. Although the gross morphology and histology of the intermolar eminence have been studied, (Owen, 1852; Livingston, '56; Cave, '77), its function is poorly understood. Sonntag ('25) believed its purpose was to raise the food up to the level of the grinding teeth. Livingston ('56) presumed that the intermolar eminence was associated with thorough mastication found in lagomorphs. An-
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other view was that this "dorsal shield" prevented passage of food from one side of the mouth to the other (Ardran et al., '58), which could be caused by the "bunching" of the tongue against the palate (Doran, '75). However, the functional movement of the intermolar eminence has not been described. One of the techniques used to study tongue movement during intraoral food transport involves fluorographic recordings of feeding animals from lateral and/or dorso-ventral views. Cinefluorographyallows changes in jaw position to be measured, and also permits the position of other structures (e.g.,tongue, hyoid) to be determined (Hiiemae,'67). Metallic markers are sometimes inserted into different parts of the masticatory structures to aid in their visualization or to create stable reference points from which to measure (Hiiemae and Crompton, '71; Thexton, '80; de Gueldre and de Vree, '84; Anapol, '88). Unfortunately, most cinefluorographic studies have been based solely upon lateral recordings, and markers were seldom employed. The movement
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of the tongue was not seen directly, but inferred from the position and direction of the stream of chewed material. The purpose of the present study was to describe the movement of the tongue as a whole, and to ascertain the function of the intermolar eminence during intraoral food transport in the rabbit (Oryctolagus cuniculus) by viewing separate lateral and dorso-ventral videofluorographic views of feeding rabbits. Metallic markers were inserted into the tongue so that movement of its various parts could be clearly seen. MATERIALS AND METHODS
Sample and marker placement We studied the movement of the tongue and intermolar eminence in six young domestic rabbits (1.53.0 kg). The rabbit was chosen because a great deal is known about rabbit mastication, it is easy to handle, and it is a convenient size for viewing videofluorographicimages. To insert the markers into the tongue, the rabbits were anesthetized with intramuscular ketamine (35 mg/ kg) and xylaxine ( 5 mg/kg). Once anesthetized, the rabbits’ jaws were opened manually to expose the tongue. Pieces of barbed gold dental root canal broach (Crescent Dental Mfg. Co., Lyons, IL 60534), 1 . 5 3 mm in length and 1mm in diameter, were inserted into several areas of the tongue in each of the six animals. These markers were inserted with a hypodermic needle. Gold dental broach was used because of gold’s radiopacity and inertness, and because we expected that the barbs would stabilize the marker. In three animals, three metal markers were inserted into the midline of the tongue. These markers were all 1.5 mm in length and were inserted, one each, in the anterior, middle, and posterior portions of the tongue. In another three animals, four markers of varying sizes were inserted at the lateral border of the intermolar eminence. Two markers 3 mm in length were inserted into the left lateral anterior and left lateral posterior portions of the intermolar eminence. The remaining two markers, 1.5 mm in length, were inserted into the right lateral anterior and right lateral posterior portion of the intermolar eminence. The difference in size of the markers allowed us to distinguish left from right markers in the lateral view.
lateral aspect prior to the insertion of any markers to create a baseline for comparison. There was no observable change in feeding activity after insertion of the markers. The chewing rate before and after marker insertion was 4.0 * 0.32 (mean t S.D.) cycles per second, and gape remained within the normal range of 11-14’. Within 2 weeks following the placement of markers, the rabbits were videofluorographed a second time with a Philips Diagnost C fluoroscope unit (Philips Medical Systems, Shelton, CN 06484). The image intensifier of the fluoroscope was connected to a videotape recorder to capture the image. By moving the c-arm on the fluoroscope unit, we could fluorograph the rabbits from separate lateral and dorso-ventral views.
Measurements and calculations Movement of the tongue was analyzed in both sagittal and horizontal planes by observing the rabbit’s chewing cycle at normal speed and in slow motion on the videotape. Sequences were selected in which visual observation could confirm relatively constant head position and that the mid-sagittal plane of the subject was parallel to the image intensifier. Still frames (1/30 second time interval) of the video image were viewed and certain points were digitized using a L-W International Model 110 Photo-Optical Digitizer (L-W International, Woodland Hills, CA 91367) with a video monitor. Digitizing began on a frame in which the rabbit was believed to be at maximum intercuspation. The videotape was then advanced manually one frame at a time until at least five continuous chewing cycles were digitized. Chewing cycles were similarly analyzed in each of the animals. Figure l a illustrates the points on the skull from a lateral view that were digitized from the videotape frames: A) the intersection of the most anterior maxillary cheek tooth and the palate; B) the intersection of the palatal surface of the maxillary incisor and the palate; C) a line perpendicular to line AB passing through the tip of the maxillary central incisor; D) the intersection of the most anterior mandibular cheek tooth and the alveolus; E) the intersection of the lingual surface of the mandibular incisor and the alveolus. Thus, the line AB represents the hard palate, and DE represents the mandibular alveolar plane. The following measurements were made Videofluorographic technique for each lateral video field: 1)mandibular gapeEach subject was fed pelletized chow in a the angle of the palatal plane with the mandibuspecialized feeding cage that limited lateral lar alveolar plane; 2) anterior-posterior position movement of the head (Muhl and Newton, ’82). of the tongue relative to the maxillary central The rabbits were videofluorographed from the incisor-distance from each midline and lateral
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a
Fig. 1. Points on skull that were digitized for videofluorographic analysis (see Materials and Methods for details): a: Lateral aspect. b Dorso-ventral aspect.
intermolar eminence marker normal to line C; 3) vertical position of the tongue relative to the palatal plane-distance from each midline and lateral intermolar eminence marker normal to line AB; 4) change in length of the tonguechange in length between midline markers and between lateral markers. These measurements allowed the sequential plotting of changes in 1) mandibular gape and 2) antero-posterior and dorso-ventral movement of the tongue and intermolar eminence relative to the maxillary incisors and the palatal plane. Figure l b illustrates the points on the skull from a dorso-ventral view that were digitized from the video image: A B ) the nasal septum delineated by point A anteriorly (superimposition of the maxillary centrals and the nasal septum) and arbitrary point B posteriorly; C'D) the
lateral surface of the right mandibular corpus delineated by arbitrary points C' anteriorly and D' posteriorly; and E ) the point of greatest concavity of the right zygomatic bone. The following measurements were made for each dorso-ventral field: 1) lateral movement of the mandible during a chewing cycle-linear change between line C'D and point E'; 2) change in width of the intermolar eminence-distance between right and left lateral intermolar eminence tongue markers. The motion of the tongue was also related to the concomitant stage in the chewing cycle. Using the convention set forth by Hiiemae ('78), the chewing cycle was divided into three component parts or strokes: 1)opening stroke (0s); 2) closing stroke (CS); and 3) power stroke (PS). The difficulty in determining the duration of the three strokes in the chewing cycle for the dorsoventral recordings of mandibular lateral excursions was obviated by using the observations drawn from Morimoto et al. ('85). They found the power stroke in rabbits can be demarcated from the closing stroke at the most lateral position of the jaw closing path, and that the temporal ratio of opening stroke:closing stroke:power stroke = 5:2:3. However, because the framing rate used in the present study was low (30 frames per second), the frame numbers in each of the figures do not correspond exactly to this ratio. Data analysis The x-y coordinates were transferred onto the computer system (IBM 3081K64) of the University of Illinois at Chicago. A general coordinate analysis program (Cleall and Chebib, '71) was then used to standardize the sets of digitized coordinate points and to calculate the specified linear and angular measurements. These data were then transferred into a Statistical Analysis System data file (SAS Institute, Cary, NC) so that a SASIGraph program could generate descriptive graphs of tongue and jaw movement and the functional movement of the intermolar eminence. RESULTS
Videofluorographic findings Viewing the videotapes at both normal and slow speed showed that tongue movement within and between animals was consistent and similar. Analysis of the digitized graphic data of 42 chewing cycles in the lateral view and 30 chewing cycles in the dorso-ventral view demonstrated that tongue movement was identical in direction in all chewing cycles. Thus a generalized account of tongue movement could be given.
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Tongue movement from the lateral view While the teeth move apart in the opening stroke the anterior and middle parts of the tongue lower and protrude (Fig. 2a,b) and the intermolar eminence elevates against the palate and protrudes (Fig. 3a,b). The distance between the anterior and posterior tongue decreases in length during the opening stroke (Fig. 4). During the closing stroke the anterior and middle parts of the tongue elevate and retract (Fig. 2a,b). The anterior intermolar eminence lowers from the palate sooner than the posterior intermolar eminence (Fig. 3a). The intermolar eminence also retracts at this time (Fig. 3b). The distance between the anterior and posterior tongue increases in length during the closing stroke (Fig. 4). During the power stroke the anterior and middle parts of the tongue are at their most elevated and retracted position (Fig. 2a,b), whereas the intermolar eminence is farthest from the palate and most posterior (Fig. 3a,b). The anterior part of the intermolar eminence reaches its lowest position in the mouth earlier in the chewing stroke than does the posterior part of the intermolar eminence (Fig. 3a).
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Tongue movement from the dorso-ventral view As the teeth move apart during the opening stroke, the mandible remains relatively centered. During this time the tongue appears to move in synchrony with all mandibular excursions (Fig. 5a,b). The intermolar eminence increases in width very slightly during the opening stroke (Fig. 6). As the closing stroke begins, the mandible moves laterally and the entire tongue and intermolar eminence move in the same direction as the laterally displaced mandible (Fig. 5a,b). The transverse dimension of the intermolar eminence remains the same as during the opening stroke (Fig. 6). The power stroke begins at the most lateral position of the mandible and is completed as it returns to the midline. So, too, the entire tongue
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Fig. 2. Representative plot of gape and movement of midline markers from the lateral view for two consecutive chewing cycles. Lines labeled “Posterior,” “Middle,” and “Anterior” represent the posterior, middle, and anterior midline tongue markers, respectively. a: Vertical marker movement with respect to the palatal plane. b Horizontal marker movement with respect to the maxillary central incisor. Vertical bars a t left of the plot indicate 5’ of gape (upper bar) and 5 mm of marker movement (lower bar). Unlabeled vertical reference lines have been placed to divide the chewing cycles into opening stroke (OS), closing stroke (CS), and power stroke (PS).
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and intermolar eminence are most lateral and moving toward the midline (Fig.5a,b).The transverse dimension of the intermolar eminence is a t its narrowest in the power stroke (Fig. 6). DISCUSSION
The movement of the tongue of the rabbit during chewing is described objectively by the data presented in Figures 1-6. However, this information offers only a partial picture of the motion of the tongue. The following paragraphs offer a more generalized description of tongue activity, based upon the frame-by-frame analysis of the movement of the markers. Where possible, a subjective interpretation of what the tongue may be doing is suggested.
Tongue movement from the lateral view During the opening stroke as the mouth opens the forepart of the tongue (anterior to the intermolar eminence) lowers from the palate and protracts. A t the same time the intermolar eminence elevates and protracts against the hard palate. As the jaws begin to close, the anterior tongue elevates and retracts while the intermolar eminence lowers and retracts. This anteriorto-posterior undulating motion may allow for movement of the food onto the intermolar eminence and in the vicinity of the cheek teeth. During the power stroke the intermolar eminence is at its lowest position when the forepart of the tongue apposes the palate. Ardran et al. (’58) stated that the forepart of the tongue moved up and backwards during the opening stroke and that the area of the tongue opposite the cheek teeth (intermolar eminence) was lowered to the level of the lower teeth when the mouth was nearly wide open. This action was then reversed on closure. These movements are inconsistent with the findings of this present study. The inconsistencies may be explained in part by the fact that the rabbits in the aforementioned study were feeding on grass. Weijs and Dantuma (’81) have shown that the amount of jaw movement changes with the type of food being chewed, and this could have an effect on tongue movement. Perhaps more importantly,
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Fig. 3. Representative plot of gape and intermolar eminence marker movement from the lateral view for two consecutive chewing cycles. Lines “A-L,” “A-R,” “P-L,” and “PR,” represent the anterior left, anterior right, posterior left, and posterior right intermolar eminence markers, respectively. a: Vertical marker movement with respect to the palatal plane. b Horizontal marker movement with respect to the maxillary central incisor. Vertical bars and reference lines are the same BS in Figure 2.
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Fig. 4. Representative plot of gape and change in length between midline markers from the lateral view for two consecutive chewing cycles. Line “A-P” represents the change in distance between the anterior and posterior midline markers. Vertical bars and reference l i e s are the same as in Figure 2.
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tongue movement in the study by Ardran et al. (’58)had to be deduced through visualizing food movement because the tongue could not be seen. Ardran et al. (’58)believed that the intermolar eminence apposed the palate during the power stroke and thereby acted as a shield, preventing the passage of food to the opposite side of the mouth. The intermolar eminence certainly acts as a shield during the opening stroke as it apposes the hard palate. However, during the closing stroke the intermolar eminence lowers from the palate and cannot be considered a shield against food passage, as Ardran suggested, because it does not appose the palate. An explanation of why food remains on one side of the mouth while the rabbit is chewing could be that food is squeezed by the teeth onto the lowered intermolar eminence during the power stroke and is then replaced onto the teeth when the intermolar eminence moves up against the palate during the opening stroke. The anterior-to-posterior undulating motion may allow for the passage of food posteriorly. Even though the bolus was not visible in the present study, it is possible that as food first enters the mouth it is placed on the forepart of the tongue. The food is then retracted by tongue
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Fig. 5. Plot of mandibular excursion and excursive movement of markers from the dorso-ventral view for two consecutive chewing cycles. Line labeled “Excursion” is the linear measurement between the lateral surface of the mandibular corpus and the point of greatest concavity of the zygomatic bone. Markers are plotted with respect to the nasal septum. a: Animal with midline markers. b Animal with lateral intermolar eminence markers. Vertical bars at left of the plot indicate 5 mm of excursion (upper bar) and 5 mm of marker movement (lower bar). Vertical reference lines are the same as in Figure 2.
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Fig. 6. Plot of mandibular excursion and change in width between intermolar eminence markers from the dorsoventral view for two consecutive chewing cycles. For explanation of lime labeled “Excursion,” see legend to Figure 5. Lines labeled “anterior,” and “posterior” represent the change in distance between the left and right anterior and posterior intermolar eminence markers. Vertical bars at left of the plot indicate 5 mm of excursion (upper bar) and 5 mm of marker movement (lower bar). Vertical reference lines are the same as in Figure 2.
movement (Ardran et al., ’58). The anterior tongue raises while the posterior tongue lowers and allows for food to be placed on the grinding teeth much as Sonntag (’25) surmised. Like the base of the tongue in the bat, macaque, and cat, the rabbit’s intermolar eminence has the same pattern of movement as reported by Anapol (’88) for the rabbit hyoid. Both intermolar eminence and hyoid move anterodorsally during the opening stroke and posteroventrally during the closing stroke, whereas the forepart of the tongue moves anteroventrally and posterodorsally during the opening and closing strokes respectively.
Tongue movement from the dorso-ventral view Prior to the present study a description of transverse motion of the rabbit tongue was not available.We found that the entire tongue moves synchronously with all mandibular movements; that is, during the opening stroke, when there is little excursive movement of the mandible, there is little excursive movement of the tongue. With increased excursion of the mandible, as during the closing and power strokes, there is increased
excursion of the tongue. The intermolar eminence follows mandibular excursion more closely than does the anterior part of the tongue. This may be due to the extrinsic muscular attachment of the intermolar eminence to the hyoid bone and the genial tubercles. The anterior part of the tongue lags behind slightly in its excursive movement when compared to the mandible.
Inter-tongue movement The entire tongue appears to shorten in length during the opening stroke, remains relatively shorter during the closing stroke, and lengthens again during the power stroke. There appear to be three possibilities for this shortening and lengthening: 1)the first involves an actual shortening of the entire tongue, 2) another may be a relative shortening or lengthening due to a curving of the tongue around the area of the middle marker, and 3) finally, this movement may be a combination of the two. After viewing the film at different speeds, it appears that the tongue is bending in the middle. During the opening stroke the intermolar eminence widens slightly and is at its widest dimension during the closing stroke. During the power strokethe intermolar eminence shortens in width. A possible explanation of the transverse shortening of the intermolar eminence during the power stroke is that this part of the tongue is twisting to allow for food to be placed or maintained on the teeth on the working side. If this is true, then the projected measurement from the dorso-ventral view would be relative to the amount of twisting, i.e., the more twisting action of the intermolar eminence, the shorter the transverse distance between markers. This is, indeed,what was found from measurements of intermolar eminence width. CONCLUSIONS
In general, the entire tongue moves in synchrony with mandibular excursions, and exhibits an anterior to posterior undulating motion. The intermolar eminence appears to function to reposition the bolus onto the teeth during the opening stroke as it moves upward to appose the palate. During the closing and power strokes, when the tongue is not in contact with the palate, the intermolar eminence may be twisting in order to place or maintain the bolus in between the cheek teeth. ACKNOWLEDGMENTS
We would like to thank Drs. S.W. Herring and B.J. Schneider for their suggestionson this manuscript, Dr. R. Druzinsky for the invaluable assis-
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tance with digitizingthe data, and Mrs. 0.Kotov for her help in handling the animals. LITERATURE CITED Anapol, F. (1988) Morphologicaland videofluorographicstudy of the hyoid apparatus and its function in the rabbit Oryctolagus cuniculus. J. Morphol. 195:141-157. Ardran, G.M., F.H. Kemp, and W.D.L. Ride (1958) A radiographic d y s i s of mastication and swallowingin the domestic rabbit: Oryetolaguscuniculus (L). Proc. Zool. Soc. Lond. 130:257-274. Cave, A.J.E. (1977) Observations on rhinoceros tongue morphology. J. Zool. 181t265-284. Cleall, J.F., and F.S. Chebib (1971) Coordinate analysis applied to orthodontic studies. Angle Orthod. 41t214-218. Doran, G.A. (1975) Review of the evolution and phylogeny of the mammalian tongue. Acta Anat. 91t118-129. Franks, H.A., A.W. Crompton,and R.Z. German (1984) Mechanisms of intraoral transport in macaques. Am. J. Phys. Anthropol. 65:27&282. Franks, H.A., R.Z. German, A.W. Crompton, and K.M. Hiiemae (1985) Mechanism of intraoral transport in a herbivore, the Hyrax Procavia syriacus. Arch. Oral Biol. 30t539544. De Gueldre, G., and F. de Vree (1984) Movements of the mandible and tongue during mastication and swallowing in Pteropus giganteus (Megachiroptera): A cineradiographical study. J. Morphol. 179t95-114. Hiiemae, K.M. (1967) Masticatory movements in primitive mammals. In D.J. Anderson and B. Matthew (eds): Mastication. Bristol: John Wright, Paper No. 14, pp. 105-118.
Hiiemae, K.M. (1978) Mammalian mastication: A review of the activity of the jaw muscles in movements they produce in chewing. In P.M. Butler and K. Josey (eds): Studies of the Development, Structure, and Functions of Teeth. London: Academic Press, pp. 36&398. Hiiemae, K.M., and A.W. Crompton (1971) A cinefluorographic study of feeding in the American opossum, Didelphis marsupialis. In A.A. Dahlberg (ed): Dental Morphology and Evolution. Chicago: University of Chicago Press, pp. 299-334. Livingston, R.M. (1956) Some observations on the natural history of the tongue. Ann. R. CoU. Surg. Engl. 19;18&200. Morimoto, T., T. Inoue, T. Nakamura, and Y. Kawamura (1985) Characteristics of rhythmic jaw movements of the rabbit. Arch. Oral Biol. 30t673-677. Muhl, Z.F., and J.H. Newton (1982) Change in the digastric muscle length in feeding rabbits. J. Morphol. 171:151-157. Owen, R. (1852) On the anatomy of the Indian rhinoceros Rhino unicornis. Trans. Zool. Soc. Lond. 4.3-58. Sonntag, C.F. (1925) The comparative anatomy of the tongues of the Mammalia XII. Summary, classificationand phylogeny. Proc. Zool. Soc. Lond. pp. 701-762. Thexton, A.J. (1980) Tongue and hyoid movement in the cat. In Y. Kawamura and R. Dubner (eds):Oral-Facial Sensory and Motor Functions. Tokyo: Quintessence, pp. 301-312. Weijs, W.A. (1975) Mandibular movement of the albino rat during feeding. J. Morphol. 145t107-124. Weijs, W.A., and R. Dantuma (1981) Functional anatomy of themasticatoryapparatus in the rabbit. (Oryetolaguscuniculus L.) Neth. J. Zool. 31.99-147.
Videofluorographic Analysis of Tongue Movement in the Rabbit (Oryctolaguscuniculus) DAVID CORTOPASSI AND ZANE F. MUHL Department of Orthodontics, University of Illinois at Chicago, Chicago, Illinois 60612
ABSTRACT The movement of the entire tongue and intermolar eminence during mastication is described in the domestic rabbit (Oryctolagus cuniculus). Tongue movement and jaw position were analyzed videofluorographically from separate lateral and dorso-ventralviews in six rabbits. Metallic markers were inserted into the tongue so that its movement was visible on the fluorographicimage. Frame-by-frame analysis of the videofluorographictape recordings demonstrates that tongue movement in all animals was identical in direction during each part of the chewing cycle. In the lateral view the forepart of the tongue moves down and forward during the opening stroke, whereas the intermolar eminence moves up and forward to appose the palate. During the closing stroke, as the tip of the tongue moves up and back, the intermolar eminence lowersfrom the palate and retracts. During the power stroke the forepart of the tongue is at its most elevated and retruded position, while the intermolar eminence is its lowest and most retruded. The dorso-ventralview showed that lateral movement of the tongue and mandible are highly synchronous. The intermolar eminence decreases in width during the power stroke, possibly twisting to place or keep food on the teeth. An anterior to posterior undulating movement of the entire tongue occurs throughout the chewing cycle. As the intermolar eminence elevates to appose the palate during the opening stroke, it may replace the bolus on the teeth on the chewing side. The intermolar eminence also appears to be twisting during the closing and power strokes to place or maintain food on the teeth. In recent years mastication has been studied in many mammalian species,focusing mainly on the morphology of the jaws and teeth and their function in food breakdown. The function of the tongue in intraoral food transport during mastication has also been described in some mammals, e.g., for rabbits (Ardran et al., '58), bats (de Gueldre and de Vree, 'M), opossums (Hiiemae and Crompton, '71),rats (Weijs,'75), cats (Thexton, '80), macaques (Franks et al., '84)' and the hyrax (Franks et al., '85). The intermolar eminence is an elevation located on the dorsal surface of the tongue between the cheek teeth of some herbivorous ungulates, lagomorphs, and rodents. Although the gross morphology and histology of the intermolar eminence have been studied, (Owen, 1852; Livingston, '56; Cave, '77), its function is poorly understood. Sonntag ('25) believed its purpose was to raise the food up to the level of the grinding teeth. Livingston ('56) presumed that the intermolar eminence was associated with thorough mastication found in lagomorphs. An-
D 1990 WILEY-LISS,INC.
other view was that this "dorsal shield" prevented passage of food from one side of the mouth to the other (Ardran et al., '58), which could be caused by the "bunching" of the tongue against the palate (Doran, '75). However, the functional movement of the intermolar eminence has not been described. One of the techniques used to study tongue movement during intraoral food transport involves fluorographic recordings of feeding animals from lateral and/or dorso-ventral views. Cinefluorographyallows changes in jaw position to be measured, and also permits the position of other structures (e.g.,tongue, hyoid) to be determined (Hiiemae,'67). Metallic markers are sometimes inserted into different parts of the masticatory structures to aid in their visualization or to create stable reference points from which to measure (Hiiemae and Crompton, '71; Thexton, '80; de Gueldre and de Vree, '84; Anapol, '88). Unfortunately, most cinefluorographic studies have been based solely upon lateral recordings, and markers were seldom employed. The movement
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of the tongue was not seen directly, but inferred from the position and direction of the stream of chewed material. The purpose of the present study was to describe the movement of the tongue as a whole, and to ascertain the function of the intermolar eminence during intraoral food transport in the rabbit (Oryctolagus cuniculus) by viewing separate lateral and dorso-ventral videofluorographic views of feeding rabbits. Metallic markers were inserted into the tongue so that movement of its various parts could be clearly seen. MATERIALS AND METHODS
Sample and marker placement We studied the movement of the tongue and intermolar eminence in six young domestic rabbits (1.53.0 kg). The rabbit was chosen because a great deal is known about rabbit mastication, it is easy to handle, and it is a convenient size for viewing videofluorographicimages. To insert the markers into the tongue, the rabbits were anesthetized with intramuscular ketamine (35 mg/ kg) and xylaxine ( 5 mg/kg). Once anesthetized, the rabbits’ jaws were opened manually to expose the tongue. Pieces of barbed gold dental root canal broach (Crescent Dental Mfg. Co., Lyons, IL 60534), 1 . 5 3 mm in length and 1mm in diameter, were inserted into several areas of the tongue in each of the six animals. These markers were inserted with a hypodermic needle. Gold dental broach was used because of gold’s radiopacity and inertness, and because we expected that the barbs would stabilize the marker. In three animals, three metal markers were inserted into the midline of the tongue. These markers were all 1.5 mm in length and were inserted, one each, in the anterior, middle, and posterior portions of the tongue. In another three animals, four markers of varying sizes were inserted at the lateral border of the intermolar eminence. Two markers 3 mm in length were inserted into the left lateral anterior and left lateral posterior portions of the intermolar eminence. The remaining two markers, 1.5 mm in length, were inserted into the right lateral anterior and right lateral posterior portion of the intermolar eminence. The difference in size of the markers allowed us to distinguish left from right markers in the lateral view.
lateral aspect prior to the insertion of any markers to create a baseline for comparison. There was no observable change in feeding activity after insertion of the markers. The chewing rate before and after marker insertion was 4.0 * 0.32 (mean t S.D.) cycles per second, and gape remained within the normal range of 11-14’. Within 2 weeks following the placement of markers, the rabbits were videofluorographed a second time with a Philips Diagnost C fluoroscope unit (Philips Medical Systems, Shelton, CN 06484). The image intensifier of the fluoroscope was connected to a videotape recorder to capture the image. By moving the c-arm on the fluoroscope unit, we could fluorograph the rabbits from separate lateral and dorso-ventral views.
Measurements and calculations Movement of the tongue was analyzed in both sagittal and horizontal planes by observing the rabbit’s chewing cycle at normal speed and in slow motion on the videotape. Sequences were selected in which visual observation could confirm relatively constant head position and that the mid-sagittal plane of the subject was parallel to the image intensifier. Still frames (1/30 second time interval) of the video image were viewed and certain points were digitized using a L-W International Model 110 Photo-Optical Digitizer (L-W International, Woodland Hills, CA 91367) with a video monitor. Digitizing began on a frame in which the rabbit was believed to be at maximum intercuspation. The videotape was then advanced manually one frame at a time until at least five continuous chewing cycles were digitized. Chewing cycles were similarly analyzed in each of the animals. Figure l a illustrates the points on the skull from a lateral view that were digitized from the videotape frames: A) the intersection of the most anterior maxillary cheek tooth and the palate; B) the intersection of the palatal surface of the maxillary incisor and the palate; C) a line perpendicular to line AB passing through the tip of the maxillary central incisor; D) the intersection of the most anterior mandibular cheek tooth and the alveolus; E) the intersection of the lingual surface of the mandibular incisor and the alveolus. Thus, the line AB represents the hard palate, and DE represents the mandibular alveolar plane. The following measurements were made Videofluorographic technique for each lateral video field: 1)mandibular gapeEach subject was fed pelletized chow in a the angle of the palatal plane with the mandibuspecialized feeding cage that limited lateral lar alveolar plane; 2) anterior-posterior position movement of the head (Muhl and Newton, ’82). of the tongue relative to the maxillary central The rabbits were videofluorographed from the incisor-distance from each midline and lateral
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a
Fig. 1. Points on skull that were digitized for videofluorographic analysis (see Materials and Methods for details): a: Lateral aspect. b Dorso-ventral aspect.
intermolar eminence marker normal to line C; 3) vertical position of the tongue relative to the palatal plane-distance from each midline and lateral intermolar eminence marker normal to line AB; 4) change in length of the tonguechange in length between midline markers and between lateral markers. These measurements allowed the sequential plotting of changes in 1) mandibular gape and 2) antero-posterior and dorso-ventral movement of the tongue and intermolar eminence relative to the maxillary incisors and the palatal plane. Figure l b illustrates the points on the skull from a dorso-ventral view that were digitized from the video image: A B ) the nasal septum delineated by point A anteriorly (superimposition of the maxillary centrals and the nasal septum) and arbitrary point B posteriorly; C'D) the
lateral surface of the right mandibular corpus delineated by arbitrary points C' anteriorly and D' posteriorly; and E ) the point of greatest concavity of the right zygomatic bone. The following measurements were made for each dorso-ventral field: 1) lateral movement of the mandible during a chewing cycle-linear change between line C'D and point E'; 2) change in width of the intermolar eminence-distance between right and left lateral intermolar eminence tongue markers. The motion of the tongue was also related to the concomitant stage in the chewing cycle. Using the convention set forth by Hiiemae ('78), the chewing cycle was divided into three component parts or strokes: 1)opening stroke (0s); 2) closing stroke (CS); and 3) power stroke (PS). The difficulty in determining the duration of the three strokes in the chewing cycle for the dorsoventral recordings of mandibular lateral excursions was obviated by using the observations drawn from Morimoto et al. ('85). They found the power stroke in rabbits can be demarcated from the closing stroke at the most lateral position of the jaw closing path, and that the temporal ratio of opening stroke:closing stroke:power stroke = 5:2:3. However, because the framing rate used in the present study was low (30 frames per second), the frame numbers in each of the figures do not correspond exactly to this ratio. Data analysis The x-y coordinates were transferred onto the computer system (IBM 3081K64) of the University of Illinois at Chicago. A general coordinate analysis program (Cleall and Chebib, '71) was then used to standardize the sets of digitized coordinate points and to calculate the specified linear and angular measurements. These data were then transferred into a Statistical Analysis System data file (SAS Institute, Cary, NC) so that a SASIGraph program could generate descriptive graphs of tongue and jaw movement and the functional movement of the intermolar eminence. RESULTS
Videofluorographic findings Viewing the videotapes at both normal and slow speed showed that tongue movement within and between animals was consistent and similar. Analysis of the digitized graphic data of 42 chewing cycles in the lateral view and 30 chewing cycles in the dorso-ventral view demonstrated that tongue movement was identical in direction in all chewing cycles. Thus a generalized account of tongue movement could be given.
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Tongue movement from the lateral view While the teeth move apart in the opening stroke the anterior and middle parts of the tongue lower and protrude (Fig. 2a,b) and the intermolar eminence elevates against the palate and protrudes (Fig. 3a,b). The distance between the anterior and posterior tongue decreases in length during the opening stroke (Fig. 4). During the closing stroke the anterior and middle parts of the tongue elevate and retract (Fig. 2a,b). The anterior intermolar eminence lowers from the palate sooner than the posterior intermolar eminence (Fig. 3a). The intermolar eminence also retracts at this time (Fig. 3b). The distance between the anterior and posterior tongue increases in length during the closing stroke (Fig. 4). During the power stroke the anterior and middle parts of the tongue are at their most elevated and retracted position (Fig. 2a,b), whereas the intermolar eminence is farthest from the palate and most posterior (Fig. 3a,b). The anterior part of the intermolar eminence reaches its lowest position in the mouth earlier in the chewing stroke than does the posterior part of the intermolar eminence (Fig. 3a).
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Tongue movement from the dorso-ventral view As the teeth move apart during the opening stroke, the mandible remains relatively centered. During this time the tongue appears to move in synchrony with all mandibular excursions (Fig. 5a,b). The intermolar eminence increases in width very slightly during the opening stroke (Fig. 6). As the closing stroke begins, the mandible moves laterally and the entire tongue and intermolar eminence move in the same direction as the laterally displaced mandible (Fig. 5a,b). The transverse dimension of the intermolar eminence remains the same as during the opening stroke (Fig. 6). The power stroke begins at the most lateral position of the mandible and is completed as it returns to the midline. So, too, the entire tongue
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Fig. 2. Representative plot of gape and movement of midline markers from the lateral view for two consecutive chewing cycles. Lines labeled “Posterior,” “Middle,” and “Anterior” represent the posterior, middle, and anterior midline tongue markers, respectively. a: Vertical marker movement with respect to the palatal plane. b Horizontal marker movement with respect to the maxillary central incisor. Vertical bars a t left of the plot indicate 5’ of gape (upper bar) and 5 mm of marker movement (lower bar). Unlabeled vertical reference lines have been placed to divide the chewing cycles into opening stroke (OS), closing stroke (CS), and power stroke (PS).
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and intermolar eminence are most lateral and moving toward the midline (Fig.5a,b).The transverse dimension of the intermolar eminence is a t its narrowest in the power stroke (Fig. 6). DISCUSSION
The movement of the tongue of the rabbit during chewing is described objectively by the data presented in Figures 1-6. However, this information offers only a partial picture of the motion of the tongue. The following paragraphs offer a more generalized description of tongue activity, based upon the frame-by-frame analysis of the movement of the markers. Where possible, a subjective interpretation of what the tongue may be doing is suggested.
Tongue movement from the lateral view During the opening stroke as the mouth opens the forepart of the tongue (anterior to the intermolar eminence) lowers from the palate and protracts. A t the same time the intermolar eminence elevates and protracts against the hard palate. As the jaws begin to close, the anterior tongue elevates and retracts while the intermolar eminence lowers and retracts. This anteriorto-posterior undulating motion may allow for movement of the food onto the intermolar eminence and in the vicinity of the cheek teeth. During the power stroke the intermolar eminence is at its lowest position when the forepart of the tongue apposes the palate. Ardran et al. (’58) stated that the forepart of the tongue moved up and backwards during the opening stroke and that the area of the tongue opposite the cheek teeth (intermolar eminence) was lowered to the level of the lower teeth when the mouth was nearly wide open. This action was then reversed on closure. These movements are inconsistent with the findings of this present study. The inconsistencies may be explained in part by the fact that the rabbits in the aforementioned study were feeding on grass. Weijs and Dantuma (’81) have shown that the amount of jaw movement changes with the type of food being chewed, and this could have an effect on tongue movement. Perhaps more importantly,
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Fig. 4. Representative plot of gape and change in length between midline markers from the lateral view for two consecutive chewing cycles. Line “A-P” represents the change in distance between the anterior and posterior midline markers. Vertical bars and reference l i e s are the same as in Figure 2.
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tongue movement in the study by Ardran et al. (’58)had to be deduced through visualizing food movement because the tongue could not be seen. Ardran et al. (’58)believed that the intermolar eminence apposed the palate during the power stroke and thereby acted as a shield, preventing the passage of food to the opposite side of the mouth. The intermolar eminence certainly acts as a shield during the opening stroke as it apposes the hard palate. However, during the closing stroke the intermolar eminence lowers from the palate and cannot be considered a shield against food passage, as Ardran suggested, because it does not appose the palate. An explanation of why food remains on one side of the mouth while the rabbit is chewing could be that food is squeezed by the teeth onto the lowered intermolar eminence during the power stroke and is then replaced onto the teeth when the intermolar eminence moves up against the palate during the opening stroke. The anterior-to-posterior undulating motion may allow for the passage of food posteriorly. Even though the bolus was not visible in the present study, it is possible that as food first enters the mouth it is placed on the forepart of the tongue. The food is then retracted by tongue
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Fig. 5. Plot of mandibular excursion and excursive movement of markers from the dorso-ventral view for two consecutive chewing cycles. Line labeled “Excursion” is the linear measurement between the lateral surface of the mandibular corpus and the point of greatest concavity of the zygomatic bone. Markers are plotted with respect to the nasal septum. a: Animal with midline markers. b Animal with lateral intermolar eminence markers. Vertical bars at left of the plot indicate 5 mm of excursion (upper bar) and 5 mm of marker movement (lower bar). Vertical reference lines are the same as in Figure 2.
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Fig. 6. Plot of mandibular excursion and change in width between intermolar eminence markers from the dorsoventral view for two consecutive chewing cycles. For explanation of lime labeled “Excursion,” see legend to Figure 5. Lines labeled “anterior,” and “posterior” represent the change in distance between the left and right anterior and posterior intermolar eminence markers. Vertical bars at left of the plot indicate 5 mm of excursion (upper bar) and 5 mm of marker movement (lower bar). Vertical reference lines are the same as in Figure 2.
movement (Ardran et al., ’58). The anterior tongue raises while the posterior tongue lowers and allows for food to be placed on the grinding teeth much as Sonntag (’25) surmised. Like the base of the tongue in the bat, macaque, and cat, the rabbit’s intermolar eminence has the same pattern of movement as reported by Anapol (’88) for the rabbit hyoid. Both intermolar eminence and hyoid move anterodorsally during the opening stroke and posteroventrally during the closing stroke, whereas the forepart of the tongue moves anteroventrally and posterodorsally during the opening and closing strokes respectively.
Tongue movement from the dorso-ventral view Prior to the present study a description of transverse motion of the rabbit tongue was not available.We found that the entire tongue moves synchronously with all mandibular movements; that is, during the opening stroke, when there is little excursive movement of the mandible, there is little excursive movement of the tongue. With increased excursion of the mandible, as during the closing and power strokes, there is increased
excursion of the tongue. The intermolar eminence follows mandibular excursion more closely than does the anterior part of the tongue. This may be due to the extrinsic muscular attachment of the intermolar eminence to the hyoid bone and the genial tubercles. The anterior part of the tongue lags behind slightly in its excursive movement when compared to the mandible.
Inter-tongue movement The entire tongue appears to shorten in length during the opening stroke, remains relatively shorter during the closing stroke, and lengthens again during the power stroke. There appear to be three possibilities for this shortening and lengthening: 1)the first involves an actual shortening of the entire tongue, 2) another may be a relative shortening or lengthening due to a curving of the tongue around the area of the middle marker, and 3) finally, this movement may be a combination of the two. After viewing the film at different speeds, it appears that the tongue is bending in the middle. During the opening stroke the intermolar eminence widens slightly and is at its widest dimension during the closing stroke. During the power strokethe intermolar eminence shortens in width. A possible explanation of the transverse shortening of the intermolar eminence during the power stroke is that this part of the tongue is twisting to allow for food to be placed or maintained on the teeth on the working side. If this is true, then the projected measurement from the dorso-ventral view would be relative to the amount of twisting, i.e., the more twisting action of the intermolar eminence, the shorter the transverse distance between markers. This is, indeed,what was found from measurements of intermolar eminence width. CONCLUSIONS
In general, the entire tongue moves in synchrony with mandibular excursions, and exhibits an anterior to posterior undulating motion. The intermolar eminence appears to function to reposition the bolus onto the teeth during the opening stroke as it moves upward to appose the palate. During the closing and power strokes, when the tongue is not in contact with the palate, the intermolar eminence may be twisting in order to place or maintain the bolus in between the cheek teeth. ACKNOWLEDGMENTS
We would like to thank Drs. S.W. Herring and B.J. Schneider for their suggestionson this manuscript, Dr. R. Druzinsky for the invaluable assis-
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tance with digitizingthe data, and Mrs. 0.Kotov for her help in handling the animals. LITERATURE CITED Anapol, F. (1988) Morphologicaland videofluorographicstudy of the hyoid apparatus and its function in the rabbit Oryctolagus cuniculus. J. Morphol. 195:141-157. Ardran, G.M., F.H. Kemp, and W.D.L. Ride (1958) A radiographic d y s i s of mastication and swallowingin the domestic rabbit: Oryetolaguscuniculus (L). Proc. Zool. Soc. Lond. 130:257-274. Cave, A.J.E. (1977) Observations on rhinoceros tongue morphology. J. Zool. 181t265-284. Cleall, J.F., and F.S. Chebib (1971) Coordinate analysis applied to orthodontic studies. Angle Orthod. 41t214-218. Doran, G.A. (1975) Review of the evolution and phylogeny of the mammalian tongue. Acta Anat. 91t118-129. Franks, H.A., A.W. Crompton,and R.Z. German (1984) Mechanisms of intraoral transport in macaques. Am. J. Phys. Anthropol. 65:27&282. Franks, H.A., R.Z. German, A.W. Crompton, and K.M. Hiiemae (1985) Mechanism of intraoral transport in a herbivore, the Hyrax Procavia syriacus. Arch. Oral Biol. 30t539544. De Gueldre, G., and F. de Vree (1984) Movements of the mandible and tongue during mastication and swallowing in Pteropus giganteus (Megachiroptera): A cineradiographical study. J. Morphol. 179t95-114. Hiiemae, K.M. (1967) Masticatory movements in primitive mammals. In D.J. Anderson and B. Matthew (eds): Mastication. Bristol: John Wright, Paper No. 14, pp. 105-118.
Hiiemae, K.M. (1978) Mammalian mastication: A review of the activity of the jaw muscles in movements they produce in chewing. In P.M. Butler and K. Josey (eds): Studies of the Development, Structure, and Functions of Teeth. London: Academic Press, pp. 36&398. Hiiemae, K.M., and A.W. Crompton (1971) A cinefluorographic study of feeding in the American opossum, Didelphis marsupialis. In A.A. Dahlberg (ed): Dental Morphology and Evolution. Chicago: University of Chicago Press, pp. 299-334. Livingston, R.M. (1956) Some observations on the natural history of the tongue. Ann. R. CoU. Surg. Engl. 19;18&200. Morimoto, T., T. Inoue, T. Nakamura, and Y. Kawamura (1985) Characteristics of rhythmic jaw movements of the rabbit. Arch. Oral Biol. 30t673-677. Muhl, Z.F., and J.H. Newton (1982) Change in the digastric muscle length in feeding rabbits. J. Morphol. 171:151-157. Owen, R. (1852) On the anatomy of the Indian rhinoceros Rhino unicornis. Trans. Zool. Soc. Lond. 4.3-58. Sonntag, C.F. (1925) The comparative anatomy of the tongues of the Mammalia XII. Summary, classificationand phylogeny. Proc. Zool. Soc. Lond. pp. 701-762. Thexton, A.J. (1980) Tongue and hyoid movement in the cat. In Y. Kawamura and R. Dubner (eds):Oral-Facial Sensory and Motor Functions. Tokyo: Quintessence, pp. 301-312. Weijs, W.A. (1975) Mandibular movement of the albino rat during feeding. J. Morphol. 145t107-124. Weijs, W.A., and R. Dantuma (1981) Functional anatomy of themasticatoryapparatus in the rabbit. (Oryetolaguscuniculus L.) Neth. J. Zool. 31.99-147.
