Masticatory muscles of the great-gray kangaroo (Macropus giganteus)

Authors


Abstract

The great-gray kangaroo (Macropus giganteus) belongs to the Diprotodontia suborder (herbivorous marsupials of Australia) of the order of marsupials. We dissected the masticatory muscles in the great-gray kangaroo and classified them based on their innervation. Three (two male and one female) adult great-gray kangaroos (M. giganteus), fixed with 10% formalin, were examined. The masseter muscle of the great-gray kangaroo was classified into four layers (superficial layers 1, 2, 3, and a deep layer), all innervated by masseteric nerves. Layer 1 of the masseter muscle was well developed and the deep layer inserted into the masseteric canal. The zygomaticomandibular muscle, which belongs to both the masseter and temporalis muscles, was innervated by both the masseteric nerve and posterior deep temporal nerve, and the temporalis muscle was innervated by the anterior and posterior deep temporal nerves. The medial pterygoid muscle, which was innervated by the medial pterygoid nerve, was divided into superficial and deep portions. The lateral pterygoid muscle was divided into superior and inferior heads by the buccal nerve. We propose that the relationship of the masticatory muscles in the kangaroo has evolved by passive anterior invasion of the deep layer of the masseter by the medial pterygoid muscle via the masseteric canal, associated with the development of an anteroposterior mode of mastication. Anat Rec 2007. © 2007 Wiley-Liss, Inc.

The great-gray kangaroo (Macropus giganteus) belongs to the Diprotodontia suborder (herbivorous marsupials of Australia) of the order of marsupials (Marshall et al., 1990).

Lubosh (1908) described two layers of the masseter muscle and reported on the zygomaticomandibularis muscle between the masseter and temporalis muscles in the kangaroo (M. onychogale), and Lentle et al. (1998) also described two layers of the masseter muscle in the tammar wallaby (M. eugenii). Yoshikawa and Suzuki (1965) reported in detail on the masticatory muscles of the red kangaroo, classifying the deep masseter into 12 parts, and Owen (1841) described the wide canals on the ascending ramus of the mandible of the rat kangaroo.

Two monophyletic families of the superfamily Macropodoidea are recognized: Potoroidea and Macropodoidea (Flannery, 1989). Potoroidea and, to a lesser extent, Macropodoidea have a masseteric canal in their mandibular body that accommodates the insertion of the deep masseter (Lubosh, 1908; Abbie, 1939; Sanson, 1989). Potoroidea, which have a very distinct masseteric canal, display only anteroposterior occlusion, whereas Macropodoidea have acquired mediolateral occlusion as well (Sanson, 1989). The masseteric canal connects to the alveolar canal. Macropodoidea can be distinguished from other Diprotodontia by their masseteric canal (Abbie, 1939; DeBlase and Martin, 1974). The masseteric canals also provide an important criterion for classification within Macropodoidea (Archer and Bartholomai, 1978; Flannery, 1989; Ride, 1993; Wroe et al., 1998).

Abbie (1939) thought that the medial insertion of the masseter muscle in the masseteric canal aided in the production of lateral movements of the mandible reinforcing the lateral pterygoid of the opposite side. Subsequently, several researchers have postulated about the possible function of the canal and the deep layer of the masseter muscle (Friant, 1954; Ride, 1959; Sanson, 1980, 1989). However, the functional relationships of those structures are still not clear (Sanson, 1989). The purpose of this study was to dissect the masticatory muscles in the great-gray kangaroo and to classify them on the basis of their innervation. The second goal of the study was to explain the specialization of the masticatory muscles and to describe the relationship between the masseteric canal and the deep layer of the masseter.

MATERIALS AND METHODS

Three (two male and one female) adult great-gray kangaroos (Macropus giganteus), fixed with 10% formalin, were examined. We cut the necks at the level of the first cervical vertebra and the heads were cut in half in the sagittal plane. The skin was removed carefully. The superficial structures (e.g. the parotid ducts, facial artery, facial nerve) were removed and we then removed the parotid gland to identify and retain the maxillary artery. The buccal fat pad over the buccinator muscle was removed to identify and retain the buccal nerve in situ to establish topographic relationships. The zygomatic arch was removed entirely by osteotomy. We then removed the tongue from the median side and identified the lingual nerve and artery. We removed the pharynx and digastric muscle to expose the medial pterygoid muscle. We then broke the basicranium from the medial aspect with a chisel and bone rongeur to display foramen ovale and identify the root of the mandibular nerve. We identified the branches of the mandibular nerve, dissected the masticatory muscles, and also observed the intramuscular distributions of the nerves.

RESULTS

The mandible had a large pterygoid fossa on the medial side of the mandibular angle (Fig. 1). The lateral wall of the pterygoid fossa and the medial wall of the masseteric fossa were on opposite sides of a bony plate. This bony plate was inclined medially so that it divided the masseteric fossa and pterygoid fossa diagonally. The mandibular angle was inflected. The masseteric fossa was located on the lateral side of the mandibular ramus. The anteroinferior end of the fossa continued to the masseteric canal, where the deep layer of masseter inserted. The masseteric canal connected to the inferior alveolar canal and it also connected to the medial pterygoid fossa through the masseteric foramen.

Figure 1.

Dorsal aspect of the mandible of the kangaroo, slightly left view. The masseteric canal (mc) connects with the pterygoid fossa (pf) through the masseteric foramen (mfo). c, condyle; ia, inflected angle; mf, masseteric fossa; r, ramus; mcr, masseteric crest.

We cut the mandibular nerve just above the foramen ovale. The medial pterygoid nerve branched off the mandibular nerve medially (Fig. 2). The buccal nerve and the masseteric nerve arose above the otic ganglion from the mandibular nerve. The buccal nerve passed between the superior and inferior heads of the lateral pterygoid muscle. It reached the anterior part of the temporal muscle and the anterior deep temporal nerves branched off to the anterior deep portion of the temporalis muscle. The masseteric nerve passed above the superior head of the lateral pterygoid muscle. It branched into the posterior deep temporal nerves that traveled to the posterior part of the temporalis muscle and the zygomaticomandibularis muscle. It then came out from the temporal fossa over the mandibular notch and innervated the zygomaticomandibular muscle and the masseter muscle. The lateral pterygoid nerve arose from the mandibular nerve just inferior to the buccal nerve.

Figure 2.

The mandibular nerve of the kangaroo. Right side medial view. The medial pterygoid muscle has been removed. The buccal nerve (bc) passes between the superior head (sh) and inferior head (ih) of the lateral pterygoid muscle. It then branches into the anterior deep temporal nerves (at) that pass to the anterior medial surface of the temporal muscle (tm). The common trunk of the masseteric nerve (ms) branches into the posterior deep temporal nerves (pt) that enter the posterior part of the temporal muscle, then pass above the mandibular notch and branch into the masseteric nerves to masseter. aa, alveolar artery; al, alveolar nerve; au, auriculotemporal nerve; ct, chorda tympani; li, lingual nerve; lp, lateral pterygoid nerve; mh, mylohyoid nerve; pt, posterior deep temporal nerve; mp, medial pterygoid nerve; V3, mandibular nerve.

The masseter muscle of the great-gray kangaroo was divided into four layers (superficial layer 1, 2, 3, and a deep layer). The surface of superficial layer 1 was aponeurotic (Fig. 3A). It was shaped like a large rectangle, covering most of the lateral aspect of the mandibular angle. This layer originated mainly from the lateral surface of the anterior two-thirds of the zygomatic arch. The inferior fibers originated from the lateral surface of the mandibular body below the third molar tooth. This layer inserted into the inferolateral border of the mandibular angle as far posteriorly as the angular process. The muscle fibers of this layer ran anteroposteriorly and almost horizontally. It was well developed and was innervated by a masseteric nerve on the medial surface.

Figure 3.

The masseter muscles of the kangaroo. A: Superficial layer 1. B: Superficial layer 2. C: Superficial layer 3 of the masseter muscle. D: Deep layer of the masseter muscle. Superficial layer 1 ran anteroposteriorly and almost horizontally. The deeper the layers were located, the more vertically they ran. The deep layer of the masseter inserted into the masseteric canal. dm, deep layer of the masseter muscle; ia, inflected angle; ms, masseter nerve; mcr, masseteric crest; sm2, superficial layer 2 of the masseter muscle; sm3, superficial layer 3 of the masseter muscle.

Superficial layer 2 originated from the middle of the lateral aspect of the zygomatic arch (Fig. 3B) and inserted into the lateral surface of the mandibular angle around the masseteric crest. The muscle fibers of this layer ran diagonally from anterosuperior to inferoposterior. This layer was innervated by the masseteric nerve on the medial surface.

Superficial layer 3 was more vertical than the first and second layers of the masseter muscle (Fig. 3C). A thin white tendon descended from the anterior origin of the zygomatic arch and it became a fibrous aponeurosis covering the upper half of this layer. This aponeurosis was thinner than that which covered the superficial masseter. Deeper fibers arose by muscular attachment from the inferior surface of the zygomatic arch. This layer inserted into the masseteric fossa and the coronoid process of the mandible. The masseter nerve pierced it from the deep to superficial surface.

There was a masseteric canal on the lateral surface of the base of the mandibular ramus (Fig. 1) that communicated with the inferior alveolar canal through the masseteric foramen. The deep layer originated from the inferior edge of the zygomatic arch (Fig. 3D) and inserted into the masseteric fossa and the masseteric canal. The posterior part of this muscle, near the temporomandibular joint, could be distinguished from the zygomaticomandibularis muscle (Fig. 4A) by the masseter nerve, which ran between them. This muscle blended with zygomaticomandibularis muscle anteriorly. This layer was innervated by the masseteric nerve, immediately after it traveled out over the mandibular notch. As long as the insertion of the layer was located in between the intermediate layer and the zygomaticomandibularis muscle, it could not be considered to be a medial invasion but rather an anterior positioning.

Figure 4.

The masticatory muscles of the kangaroo, other than the masseter. A: Zygomaticomandibular muscle. B: Temporalis muscle. C: Lateral view of the medial and lateral pterygoid muscle. D: Ventral view of the medial and lateral pterygoid muscle. The masseteric nerve (ms) ran over the mandibular notch (mn) and between the zygomaticomandibularis muscle and the deep layer of the masseter muscle (A). The mandibular and the superficial portion of the medial pterygoid muscle have been removed to show the deep portion of the medial pterygoid muscle and the lateral pterygoid muscle (D). aa, alveolar artery; an, alveolar nerve; bc, buccal nerve; ct, chorda tympani; dp, deep portion of the medial pterygoid muscle; li, lingual nerve; lp, lateral pterygoid muscle; ma, maxillary artery; mc, masseteric canal; mcr, masseteric crest; mfo, mandibular foramen; mh, mylohyoid nerve; sp, superficial portion of the medial pterygoid muscle.

The zygomaticomandibularis muscle was fleshy and originated from the medial surface of the zygomatic arch (Fig. 4A). It inserted into the superior part of the masseteric fovea. The common trunk of the masseter nerve and the posterior deep temporal nerve innervated the zygomaticomandibularis muscle in the temporal fossa. The common trunk traveled over the mandibular notch to become the masseteric nerve outside the infratemporal fossa. The masseteric nerve ran between the zygomaticomandibularis muscle and the deep layer of the masseter muscle and innervated them. The zygomaticomandibularis muscle was innervated by the posterior deep temporal and masseteric nerves.

A dense continuous fibrous temporal fascia extended between the median sagittal crest, nuchal crest, and the zygomatic arch over the temporalis muscle. The anterolateral part was thickest in the temporal fascia. The temporal fossa comprised the frontal, parietal, temporal, and sphenoid bones and the temporalis muscle originated from the fossa, which extended from the median sagittal and nuchal crests superiorly, to the foramen ovale inferiorly. It also originated from the internal surface of the temporal fascia. The anterior group of fibers ran obliquely posteriorly, the middle group ran vertically, and the posterior group ran more anteriorly in the manner of a fan (Fig. 4B). The muscle fibers descended through the gap between the zygomatic arch and the temporal fossa and converged onto the coronoid process of the mandible to be inserted into its anterior, medial, and lateral surfaces. The posterior deep temporal nerves formed a common trunk and the masseteric nerve passed above the superior head of the lateral pterygoid muscle and traveled on the medial surface of the temporalis muscle giving off branches to it. The buccal nerve passed between the upper and lower heads of the lateral pterygoid muscle and pierced the anterior part of the temporalis muscle. The anterior deep temporal nerve innervated the temporalis muscle.

The medial pterygoid muscle had superficial and deep portions (Fig. 4C). The superficial portion originated from the medial plate of the pterygoid process of the sphenoid bone and ran vertically. It inserted into the medial aspect of the inferior margin of the mandibular angle and the inflected angle (ia in Fig. 1). This portion seemed to correspond to the medial pterygoid muscle of other animals according to its direction. The deep portion originated from the lateral plate of the pterygoid process of the sphenoid bone and the fibers ran horizontally. It inserted into the pterygoid fossa, which was located on the medial aspect of the mandibular angle. This portion was well developed and the pterygoid fossa expanded laterally at the expense of the posterior part of the masseteric fossa. This muscle was innervated by the medial pterygoid nerve, which branched off directly from the mandibular nerve (Fig. 2). As the medial pterygoid nerve arose from the mandibular nerve, we could not classify the medial pterygoid muscle into superficial and deep portions based on its the innervation.

The lateral pterygoid muscle originated from the lateral surface of the lateral lamina of pterygoid process in the sphenoid bone (Fig. 4D). It inserted into the head of the mandible and the disk of the temporomandibular joint. The buccal nerve penetrated this muscle and separated its superior and inferior heads (Fig. 2). It was innervated by the lateral pterygoid nerve, which branched off from the mandibular nerve just below the buccal nerve.

DISCUSSION

The masseter muscle of the kangaroo has been classified into 2 to 12 layers in previous studies (Abbie, 1939; Yoshikawa and Suzuki, 1965; Nakajima et al., 2000). However, the muscle layer that inserted into the masseteric canal, called the deep layer, seems to be a consistent finding in kangaroos (Abbie, 1939; Ride, 1959; Sanson, 1980, 1989; Nakajima et al., 2000; but see except for Yoshikawa and Suzuki, 1965). Superficial layer 1 of the masseter muscle was very large and ran almost horizontally anteroposteriorly. Macropodoidea have a propalinal jaw movement (Sanson, 1980, 1989), and the large superficial layer 1 of the masseter muscle may produce this anteroposterior jaw movement.

We found that the deep layer of the masseter muscle inserted into the masseteric canal and this canal connected to the inferior alveolar canal via the masseteric foramen. Potoroidea and, to a lesser extent, Macropodidae display this masseteric canal, which accommodates the insertion of the deep masseter in their mandibular body (Lubosh, 1908; Abbie, 1939; Sanson, 1989).

The zygomaticomandibular muscle dissected in this study corresponds to that reported in former studies (Yoshikawa and Suzuki, 1965; Nakajima et al., 2000). The name “zygomaticomandibular muscle” has been used for muscles that are located between the masseter and temporalis muscles (Schumacher, 1961; Yoshikawa and Suzuki, 1965; Tomo et al., 1993). As the zygomaticomandibular muscle was innervated by both the masseteric and posterior deep temporal nerves in the kangaroo, it belonged to both the masseter and temporalis muscles.

The temporalis muscle has been classified into superficial and deep layers (Yoshikawa and Suzuki, 1965) or three layers (Nakajima et al., 2000) in the kangaroo. In this study, we did not classify it into sublayers. The muscle was innervated by both anterior and posterior deep temporal nerves, consistent with previous studies (Goss, 1973; Tomo et al., 1993; Nakajima et al., 2000), so the muscle was classified into anterior and posterior parts based on its innervation.

We found that the medial pterygoid muscle had superficial and deep portions (Fig. 4C and D). The superficial portion seems to correspond to the typical medial pterygoid found in other mammals based on its direction. The relatively large pterygoid fossa in this animal was made by the deep portion (Figs. 1 and 4D). As the muscle fibers run horizontally, the deep portion may assist with propalinal jaw movement. The lateral pterygoid muscle seems small as stated formerly (Parsons, 1896; Abbie, 1939). However, compared to the carnivorous marsupials, the lateral pterygoid muscle is relatively large (Lubosh, 1908). The buccal nerve penetrated this muscle, separating the superior and inferior heads (Fig. 2). The lateral pterygoid nerve and the buccal nerve branched off from the mandibular nerve at similar levels. The lateral pterygoid muscle and the anterior part of the temporalis muscle, which were both innervated by the anterior deep temporal nerve branching from the buccal nerve, seem to belong to the same muscle group based on their innervation.

It is now usual to classify Potoroidea and Macropodoidea as different families (e.g. Archer and Bartholomai, 1978; Johnson and Strahan, 1982; Flannery et al., 1983; Strahan, 1983; Archer, 1984; Aplin and Archer, 1987; Flannery, 1989), so this implies that the masseteric canal evolved independently in these taxa. Hume (1978) studied the evolution of the digestive system within the Macropodidae and speculated that browsing macropodoids arose from potoroids, and that browsing macropodoids in turn gave rise to grazing macropodoids. Kirsh et al. (1997) retain Potoroidae and Macropodoidae as a subfamily within Macropodidae based on their DNA hybridization study.

Sanson (1978, 1989), studying masticatory cycles and dentitions, divided the macropodids into potoroid and basal macropodoid grade, browser grade, and intermediate browser/grazer grade. He has not suggested that macropodoids evolved from potoroids, only that the evolution of the macropodoid dentition has passed through three successive basic grades.

Abbie (1939) suggested that the relatively medial attachment of the deep layer of the masseter supplements the lateral pterygoid of the opposite side in the production of lateral movement. He proposed that the anterior shift of this attachment also affords increased leverage to the mandible, and this tends to compensate for the weakness engendered by the procumbency and elongation of the mandibular incisors. Fraint (1954) suggested that the function of the masseteric canal is anteroposterior mandibular movements in mastication.

Ride (1959) states that there can be no doubt that attrition is not produced by anteroposterior movements of the lower jaw as suggested by Fraint (1954). However, he supported Friant's (1954) concept of bilateral retraction of the mandible by the masseter in the masseteric canal, from the forwarding grasping position to the rearward resting position. Ride (1959) also stated there was the direct mechanical advantage to be gained by inserting the deep masseter as close as possible to the premolar. He also stated that the rotational effect of the forwardly inserted deep masseter was important in controlling the sectorial teeth. However, the orientation of the deep masseter suggests that it causes medial rotation of the mandible lingually, which would tend to disengage the premolar (Sanson, 1989).

Sanson (1980) considered that some attrition is produced by anteroposterior movement in Macropus and almost all attrition by such movements in Wallabia. Sanson (1989) proposed that the deep masseter might rotate the mandible by deflecting the lower premolar lingually away from the upper premolar. It might also act to maintain the pressure between the occluding teeth. He stated that the species with the largest premolars tend to have the best-developed deep masseter and presumably the hypertrophy of the muscle is involved in enhancing its function. He reviewed the effect of the deep masseter in the masseteric canal and stated that the effect was still not clear.

Potoroids display more development of their masseteric canal than macropodoids (Abbie, 1939; Flannery, 1989; Sanson, 1989). The former have only anteroposterior occlusion, whereas the latter have acquired mediolateral occlusion as well (Sanson, 1989). Lentle et al. (2003) confirmed these movements in the tammar wallaby by cinefluoroscopy. Potoroids evolved large sectorial premolars, which restrict mediolateral occlusion. Propalinal mandibular movement, large premolars, and a large masseteric canal are characteristic of potoroids. The masseter muscle in masseteric canal can produce bilateral retraction of the mandible from a forwarding grasping position to a rearward resting position (Friant, 1954; Ride, 1959). As the masseter in masseteric canal does not produce the protraction for propalinal movement, the effect of the masseter in masseteric canal is thought to be linked to the large premolar rather than the propalinal movement (Ride, 1959; Sanson, 1980, 1989).

We found that the deep layer of the masseter inserted into the masseteric fossa and the masseteric canal (Fig. 3D). The vertical portion of the medial pterygoid muscle inserted into the pterygoid fossa, which was located on the medial aspect of the mandibular angle (Fig. 4D).

As reported in many other mammals, the deep and superficial layers of the masseter inserted in the masseteric fossa, which was located on the lateral surface of the mandible (Fig. 5A). The masseter muscle as a whole has lateral and anterior vectors in the horizontal plane in many mammals (Turnbull, 1970). However, the deep layer of the masseter muscle displays a different vector from the superficial layers; for example, it displays a posterior vector in carnivores and herbivorous (Schumacher, 1961). We do not consider the posterior vector to be a unique direction or acquired by the anterior invasion of the deep masseter into the masseteric canal. Abbie (1939) suggested that simple superficial migration would suffice, if extra leverage were the only consideration. Sanson (1989) also described the insertion of the deep masseter into the masseteric canal to be an unusual feature. The migration of the deep masseter to a superficial location may break the layered structure of the masseter and result in an extra lateral vector to the muscle. The migration of the superficial layer (SM in Fig. 5A) to an anterior location may change the direction of the anterior vector. As the deep layer is located deep in the masseteric fossa (mf in Fig. 5A), a simple anterior shift of this layer makes a masseteric canal.

Figure 5.

Diagrammatic representation of the masseteric muscles in the kangaroo compared with those of mammals. Diagrams depict a superior view of horizontal sections of the posterior region of the right side of the mandible (circled), at about the occlusal level. A: Typical masticatory muscle location in mammals. Mandible is colored in gray. The superficial layer (SM) of the masseter muscle is located lateral to the deep layer (DM) in the masseteric fossa (mf). The medial pterygoid muscle (MP) inserts into the pterygoid fossa (pf). Arrowheads show the direction of muscle pull. The SM of masseter pulls the mandible anterolaterally in general. The MP pulls it anteromedially. The DM of the masseter pulls it posteriorly. The propalinal occlusion of the kangaroo may require the development (straight arrows) of the SM and MP to provide an anterior vector. The expansion of these muscles may squeeze out (zigzag arrow) the deep layer of the masseter anteriorly. The anterior shift (zigzag arrow) of the DM and lateral shift (large straight arrow) of the MP create the muscle relationship in B. B: The masticatory muscle relationships in kangaroos. The deep layer of the masseter is accommodated in the masseteric canal (mc). A simple anterior shift of the deep layer of the masseter creates the mc without medial shift. This shift does not change the direction of the muscle pull (white arrowheads) of DM compared with its usual location (A). The SM and DM layers of masseter still contact each other (asterisk). The DM connects to the MP via the masseteric foramen (mfo) in the kangaroo. We propose that a passive anterior migration of the deep layer of the masseter into the masseteric canal by the medial pterygoid muscle is associated with the development of an anteroposterior occlusion in the kangaroo.

The medial pterygoid muscle has medial and anterior vectors in the horizontal plane (Turnbull, 1970; Lentle et al., 1998). Abbie (1939) studied the development of the masseteric canal, masseteric foramen, and the pterygoid fossa in the Diprotodontia. He stated that the medial pterygoid enlarges first, then the deep layer of the masseter gradually extend forward. He also stated that the outcome of this sequence is that the deep part of the masseter and the medial pterygoid come to acquire an alternating insertion into the mandible. In his comparative study, the orientation of the masticatory muscles is led by the medial pterygoid muscle rather than the deep masseter muscle.

Development of an anteroposterior occlusion may result in hypertrophy (bold straight arrows in Fig. 5A) of the superficial layers of masseter and medial pterygoid muscles, which have anterior vectors in this plane. This may squeeze out (zigzag arrow) the deep layer of the masseter anteriorly in the masseteric canal of the mandible to provide greater insertion (Fig. 5B). The hypertrophy of the medial pterygoid muscle may expand its fossa as Abbie (1939) stated. The hypertrophy of the superficial layers of masseter does not seem to expand the masseteric fossa, where the muscle inserts. The medial pterygoid muscle rotates the lower premolar buccally to engage it (Sanson, 1989). As Sanson (1980) indicated, kangaroos have developed a descending process of the zygoma, where the masseter originates, rather than any projection of the mandible where it inserts. This may result in hypertrophy of the superficial layers of the masseter muscle. We propose that passive anterior invasion of the deep layer of the masseter into the masseteric canal by the medial pterygoid muscle is associated with development of an anteroposterior occlusion. The large masseteric canal and simple anteroposterior occlusion observed in potoroids appear to be consistent with this hypothesis. In contrast, the rather smaller masseteric canals in macropods might be produced by a relatively little reduced anteroposterior occlusion with extra mediolateral mandibular movement. Based on our hypothesis, none of the muscles changes their direction during evolution (white and black arrowheads in Fig. 5).

Acknowledgements

The authors thank Mr. Chris Leigh, Department of Anatomical Sciences, Medical School, Faculty of Health Sciences, University of Adelaide, for providing the specimens. Part of the work was conducted in the South Australian Museum and the authors thank Dr. Catharine Kemper for all her help.

Ancillary