Orbicularis oris and buccinator as a sphincter complex of the oral fissure – re-evaluation using isolated muscle specimens.

doi:10.21203/rs.3.rs-3771224/v1

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Orbicularis oris and buccinator as a sphincter complex of the oral fissure – re-evaluation using isolated muscle specimens.

https://doi.org/10.21203/rs.3.rs-3771224/v1

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published 04 Apr, 2024

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Purpose This study aimed to clarify the structural arrangement of the orbicularis oris (OOr), the buccinator (BC), and the other perioral muscles around the modiolus.

Methods The perioral muscles in seventeen faces were dissected in situ and/or in isolated muscle specimens, and their layers were reconstructed schematically upon pantomographic view of the skeleton to evaluate their actions.

Results The BC was composed of three parts including upper and lower oblique parts (BC-UO, BC-LO) in its superficial layer and a middle transverse part (BC-MT) in its deep layer. The superior and inferior OOr (SOOr and IOOr, respectively) were composed of an inner marginal part (SOOr-IM, IOOr-IM) and an outer labial part (SOOr-OL, IOOr-OL) in each. The perioral muscles as a whole were arranged in three layers. The first layer, with the depressor anguli oris (DAO) connected at the modiolus with the SOOr-OL, could mainly depress and deform the upper lip, as well as move the modiolus medially, upward, or downward. The second layer, with the BC-UO and the BC-LO connected at the modiolus with the IOOr-OL, could mainly elevate and deform the lower lip, as well as move the modiolus medially or laterally. The third layer, with the BC-MT continuous with the SOOr-IM, IOOr-IM, and IOOr-OL, could bring the upper and lower lip margins nearer to close the oral fissure lightly.

Conclusions The actions of the individual perioral muscles on the movement of lips were predicted to open and close the oral fissure, and widen and narrow the lip width.

orbicularis oris

buccinator

modiolus

isolated muscle specimens

lip movement

The orbicularis oris (OOr) is the main controller of the movements of the lips, and the reflexive and/or voluntary movement vitally important in food intake and the articulation of sound and speech [7, 17]. Structurally the OOr is coupled with the buccinator (BC) and the other perioral muscles at the modiolus near the angle of mouth and constitutes a functional continuum with them [20]. The anatomy of the OOr has been evaluated as an important basis for the craniofacial surgery including the repair of cleft lip [2], and for oral motor therapy and speech therapy in rehabilitation [14, 25].

The perioral muscles including the OOr are arranged radially around the angle of mouth and connected to the modiolus, which is a dense, compact mass of mobile fibromuscular tissue. Since the first detailed study by Lightoller, the modiolus has been regarded as the central hub of perioral muscles to transmit tensions and control labial movement [12, 26]. Recent anatomical studies reported some new findings that refine the anatomy of the perioral muscles especially on the inferior bundles of the BC [9], and the incisibus labii superioris (ILS) [10]. However, it has not been adequately considered how the entire perioral muscles would function as a system around the central hub of the modiolus.

The structure of the modiolus itself has been well investigated. Yu et al. studied the histological structure of the modiolus and confirmed existence of a tendinous structure in the central region of modiolus [27]. Sun et al. studied the minute structure of the modiolus with micro-CT, and clarified the continually oriented course of muscle fibers within the modiolus [21]. Thus, it would be reasonable to expect that the perioral muscles including the OOr and the BC are connected in series with each other at the modiolus, but their interrelationships are still obscure.

Recent studies on the skeletal muscles by the present authors have shown the usefulness of isolated muscle specimens to analyze the arrangement of muscle fascicles in the muscle body to provide essentially important information for the mechanical function of the muscles [11, 16, 22]. The facial muscles have scarcely been studied utilizing isolated muscle specimens, except in old anatomical atlases [3, 19]. In the present study, we analyzed the structure of the OOr, the BC, and the other perioral muscles together with the modiolus through observations on the muscle in situ as well as observation of isolated muscle specimens from both the superficial and deep aspects, and schematically reconstructed the perioral muscles based on the pantomographic view of the skeleton to evaluate the actions of the individual muscles.

All cadavers examined were from persons who had donated their bodies to Juntendo University School of Medicine for medical education and research. Prior to donation, written consent was obtained from the individuals and families. The protocol for the present research project was approved by the Ethics Committee of Juntendo University School of Medicine (approval No. 2014138).

Seventeen faces with facial muscles were collected from embalmed Japanese cadavers (11 males, 6 females; average age, 81.4 years). After analyzing the superficial aspect with the muscle in situ, the isolated specimens were harvested and cleaned by removing loose connective tissues and fat, and were observed both on the superficial and the deep aspects. The origin and insertion of the muscles were identified by combined observation of the deep surface of the isolated specimens and of the remaining naked skull. The courses and continuities of muscle fascicles were observed in the isolated specimens both on the superficial and the deep aspects. No evidence of any significant pathology, surgical procedures, or traumatic lesions to the facial muscles was seen in any of the cadavers examined.

The individual perioral muscles were schematically reconstructed on the skeletal framework of the upper and lower jaws to show the perioral muscles on a flat plane. Drawings of the skeletal framework were prepared from pantomographic X-ray images and photographic images of actual skeletons.

1. In situ dissections and observations of perioral muscles
When the perioral muscles surrounding the oral fissure were dissected and observed in situ, the superficial muscles including the platysma (PL) and zygomaticus major (Zmj) were obviously visible, attaching themselves to the modiolus from the lateral side. The depressor anguli oris (DAO) came upward to the modiolus from the inferior side, and the superior orbicularis oris (SOOr) ran upward from the modiolus to the superior lip. The DAO and SOOr were relatively robust and connected in series with each other at the modiolus area. The levator muscles of the upper lip including the levator labii superioris (LLS) were seen superior to the SOOr. The depressor labii inferioris (DLI) was apparent in the lower lip region and covered most of the inferior orbicularis oris (IOOr). (Fig. 1)

The BC was only partly visible in dissections in situ, its origin regions were concealed by the masseter and the ramus of mandible, and its termination hidden by the superficial layer of the modiolus muscles. To visualize the whole body of the BC, it was advantageous to utilize the preparations of isolated muscle specimens of the perioral muscles. (Fig. 2)

2. Layered structure and origin regions of BC

The isolated perioral muscle specimens made it possible to analyze the layered structure of the BC in four parts and their relation with the origin regions. In the deep aspect of the specimens, the middle transverse part of the BC (BC-MT) arising from the pterygomandibular raphe was clearly visible running through the deep side of the modiolus and continuing to become the OOr. In the superficial aspect, the upper oblique part (BC-UO) running downward from the maxilla and the lower oblique part (BC-LO) running upward from the mandible were observed to converge at the modiolus. In some specimens, the lowest transverse part of the BC (BC-LT) was visible in the most superficial layer to run along the lower margin of the mandible. (Figs. 2, 3)

The origin regions of the BC extended in wide swaths to include the maxilla, the pterygomandibular raphe, and the mandible, and could be related to the four parts of the BC. The BC-UO in the superficial layer arose from the maxilla at the outer surface of the alveolar process of the molar teeth. The BC-MT in the deep layer arose from the pterygomandibular raphe, extending from the hamulus of the medial pterygoid plate and the retromolar fossa of the mandible. The BC-LO in the superficial layer arose from the mandible at the outer surface of the alveolar process of the molar teeth. The BC-LT in the most superficial layer arose superficially from the same region as the BC-LO. (Figs. 2, 3)

3. Connection and continuation of the SOOr and the IOOr from the DAO and the BC

The isolated perioral muscle specimens demonstrated in the superficial aspect that SOOr was mainly connected via modiolus to the DAO, and in the deep aspect that the IOOr was mainly continuous directly to the BC-MT. It also became evident that both the SOOr and the IOOr each consisted of two distinct parts. The inner marginal part (the SOOr-IM and the IOOr-IM) along the labial margin was composed of assembly of densely packed fascicles. The outer labial part (the SOOr-OL and the IOOr-OL) making up the body of the lips was composed of loosely arranged fascicles. To analyze the connection and continuation of the two parts of the SOOr and the IOOr from the DAO and the BC, the isolated specimens have to be dissected to expose the deeper layers of muscles by removing the more superficial layers step by step. (Figs. 2, 3)

In the first step from the superficial aspect, when the superficial layers of muscles were reflected upward and removed, the DAO was firmly connected to the modiolus area, which was extended from level of angle of mouth downward about one third to the mandibular base. Thus the extent of the modiolus area could be identified by inspecting the attachment of the perioral muscles during manipulation, but could not be isolated and visualized by the removal of the muscles. In the second step, when the superficial layer of muscles was removed, the BC-UO and the BC-LO were exposed to connect to the IOOr via the modiolus area. In the third step, when the DLI covering the IOOr was removed, the IOOr-OL connecting via the modiolus from the BC-UO and the BC-LO was totally exposed. (Fig. 3)

In the deep aspect of isolated muscle specimens, the BC-MT in the deep layer was observed to branch into three streams of bundles at the angle of mouth. The first stream continued to the SOOr-IM, the second stream to the IOOr-IM, and the third stream constituted the lower bundles of the IOOr-OL. The other bundles of the IOOr-OL coming from the modiolus and connecting to the BC-UO and the BC-LO were observable in the space between the bundles from the BC-MT. (Fig. 4)

The deep aspect of isolated muscle specimens revealed that the outermost bundles of the SOOr-OL attached to the skeleton near the nostrils, representing the ILS. It was also observed that the lower bundles of the IOOr-OL attached to the skeleton near the origin of mentalis (MN), representing the incisivus labii inferioris (ILI). The bundles of ILS attaching themselves to the modiolus may be regarded either as a part of SOOr or as an independent levator of the upper lip. The bundles of the ILI could be regarded as a part of the IOOr that came from the modiolus and connected with the BC-LO, and in part directly continued from the BC-LT.

4. Reconstruction of the perioral muscles on the pantomographic framework

The graded dissection and observation of the isolated muscle specimens revealed that the main framework of perioral muscles was arranged in three layers. Layer 1 was composed of the DAO connected at the modiolus with the SOOr-OL. Layer 2 contained the BC-UO and the BC-LO connected at the modiolus with the IOOr-OL with ILI. Layer 3 was formed by the BC-MT continuous with the SOOr-IM and the IOOr-IM and the lower bundles of the IOOr-OL. The three layers of the perioral muscles were schematically depicted on the pantomographic framework of skeleton with origin area of the BC (the maxilla, pterygomandibular raphe, and mandible), with the oral fissure, the modiolus and the MN as landmarks. (Table 1, Fig. 5)

The schematic reconstruction of the perioral muscles enabled one to predict the action of muscles in the individual layers. Layer 1 would mainly depress and deform the upper lip, and in addition move the modiolus medially or upward or downward. Layer 2 would mainly elevate and deform the lower lip, and in addition move the modiolus medially or laterally. Layer 3 would bring the upper and lower lip margins nearer to close the oral fissure lightly.

1. The arrangement of the perioral muscles and the modiolus re-evaluated

The present study revealed novel and important findings on the structure of the perioral muscles, which would provide fundamentally new interpretation of the functional role in movement of the lips. As for the first point, the fascicles of the SOOr-IM and the IOOr-IM continued directly from the BC-MT and arose from the pterygomandibular raphe. On the other hand, the fascicles of the SOOr-OL and the IOOr-OL were connected at the modiolus with the other perioral muscles of different directions and origins. Those of the SOOr-OL were connected at the modiolus almost in vertical direction with the DAO arising from the lowest region of the mandible, whereas those of the IOOr-OL were almost in transverse direction either directly continuous with BC-MT or connected at the modiolus with the BC-UO and the BC-LO. (Fig. 5)

Among the modern textbooks of anatomy, the perioral muscles were most thoroughly described by Standring [20] and Tillmann and Töndury [24]. According to their descriptions, the BC inserted into the modiolus and connected to the SOOr and the IOOr in a complicated manner. In short, in the middle portion of the BC, the vertical decussation at the angle of mouth, and their upper and lower halves were inversely connected to the IOOr and the SOOr, repectively, while highest and lowest portions of the BC were connected without decussation to the SOOr and the IOOr, respectively. In addition, the SOOr was connected also with the DAO, and the IOOr was connected also with the Zmj and the levator anguli oris (LAO). The depicted arrangement was symmetrical vertically to the modiolus and was hypothesized to be the location of the modiolus at the level of the angle of mouth. On the other hand, the present study clarified that the modiolus was located lower in the mandibular region, and that the perioral muscles were arranged asymmetrical vertically. Indeed, the SOOr-OL was connected at the modiolus with the DAO in the vertical direction, whereas the IOOr-OL (including the ILI) was either connected or continuous with the BC horizontally.

2. Historical background of the BC and OOr anatomy

The current understanding of the arrangement of perioral muscles was formed substantially following the classical anatomy textbooks in the 19th and 20th centuries. In the older textbooks, such as Gegenbaur [5], Gray and Lewis [6], Merkel [13], Poirier, [15], Schäfer and Thane [18], Testut [23], OOr and BC were regarded to be continuous with each other and arranged vertically symmetrical to the angle of mouth between the upper and lower halves. (Online Resource 1)

Isolated muscle specimens of the facial muscles were depicted in the anatomical atlases of Bonamy et al. [3] and Spalteholz [19]. In these figures showing the deep aspect of the perioral muscles, the continuation of the muscle bundles between the BC-MT and the IOOr is beautifully depicted. It is noteworthy that the illustration of Spalteholz [19] clearly shows the branching and continuation of the BC-MT into the SOOr-IM and the IOOr-IM and into the lower bundles of the IOOr-OL, which is a point consistent with the present study. Since then, however, these observations were not well appreciated, and gradually forgotten. (Online Resource 2)

The classical concept of perioral muscle architecture hypothesizing the continuation of the OOr and the BC had to be completely reconsidered by the study of Lightoller [12] on the modiolus, which had been known by German anatomists as the “Knoten” indicating a dense compact mass near the angle of mouth. Lightoller reported that a number of perioral muscles converge towards the modiolus, and that the modiolus extended from the apex at the muscular surface to the base adjacent to the oral mucosa, implying that the fascicles of the BC and the OOr were completely interrupted at the modiolus [12]. Thereafter, the modern English and German textbooks [20, 24] emphasized the modiolus as a connecting focus for the perioral muscles, and admitted the interruption of the fascicles between BC and OOr. The present findings reappraised the classical concept of continuation of the fascicles between the OOr and the BC, and revealed that the fascicles were in part directly continuous and in part indirectly connected at the modiolus.

The location of the modiolus was not precisely evaluated by Lightoller [12], and thus roughly assigned near the angle of mouth following the classical scheme admitting decussation of the perioral muscles at the angle of mouth. Modern anatomy textbooks [20, 24] admitted the location of the modiolus to be at the angle of mouth in general. The location of the modiolus was analyzed so far by identifying firm core of the modiolus in cadaveric dissection, and was reported to be 10-20 mm lateral and 0-10 mm below the oral commissure [1, 4, 8, 27]. However, since the modiolus was a dense compact fibromuscular mass of considerable size, in the present study we employed another approach to identify the location and dimensions by defining the modiolus area where the perioral muscles adhered with each other around the modiolus core. It was thus shown that the modiolus area was not localized near the angle of mouth, but extended from the level of angle of mouth downward about one third to the base of mandible. The downward extension of the modiolus area from the angle of mouth was favorable to linking the BC-UO and the BC-LO to the IOOr-OL, and was related to the vertical asymmetry of the perioral muscles discovered in the present study.

The ILS may be regarded as an accessory muscle of the SOOr [20]. Since the ILS arose from the incisive fossa of the maxilla and its fascicles blended into the SOOr-OL and the LAO to insert into the modiolus [10], it would be functionally different from the SOOr-OL and could elevate the modiolus. The ILI may be regarded as an accessory muscle of the IOOr [20], that is attached laterally to the modiolus and medially to the incisive fossa of mandible near the origin of MN. The ILI would functionally almost equivalent to the IOOr-OL. The fascicles of the BC-LT were observed in at least 35% of the cases and were continuous with the ILI, according to Hur et al. [9].

3. Predicted actions of perioral muscles on the lip

The open and closed positions of the oral fissure should be seen as frequently linked with jaws. The action of the perioral muscles on the lips can be reasonably predicted on the basis of the anatomy of the BC and the OOr as revealed in the present study, either with moving jaws or with stationary jaws. (Table 2, Fig. 6)

During the movement of the jaws, the lips can open or close easily by following the jaws, without active shortening or passive extension of the perioral muscles (Case 1, Fig. 6a). When the jaws are to open with the lips closed, the height of both the lips should increase and the lip width should be decreased, and layer 1 (the SOOr-OL, the DAO) would be extended passively, while in layer 2, the IOOr-OL would shorten actively and the BC-UO and the BC-LO would be extended passively (Case 2, Fig. 6b). When the opened jaws are to close again with the lips closed, the three layers of muscles would be relaxed (Case 3, Fig. 6c). (Table 2)

During stationary position of jaws, the lips may open and close, and the lip width may widen or narrow. When the lips are to open with stationary jaws, the upper lip should be elevated by active shortening of the LLS and the lower lip should be depressed by active shortening of the DLI, whereas the three layers of muscles would be relaxed (Case 4, Fig. 6d). When the lips are to close lightly with stationary jaws, the upper lip margin should be lowered and the lower lip margin should be raised slightly by active shortening of Layer 3 including the SOOr-IM and the IOOr-IM, whereas both the LLS and the DLI would be relaxed (Case 5, Fig. 6e). When the lips are to close strongly associated with the deformation of lips, the whole upper lip should be depressed and the whole lower lip should be elevated powerfully by active shortening of the SOOr-OL in layer 1, IOOr-OL in layer 2 and layer 3, whereas the DAO in layer 1 and the BC-UO and the BC-LO in layer 2 should be statically tensed, and the LLS and the DLI should be extended passively (Case 6, Fig. 6f). When the lip width is to be widened, the modiolus should be abducted by active shortening of the BC-UO and the BC-LO in layer 2 and of the Zmj and the PL with static tension of the MN, whereas the IOOr-OL in layer 2 should be passively extended (Case 7, Fig. 6g). When the lip width is to be narrowed, the modiolus should be adducted by active shortening of SOOr-OL in layer 1 and the IOOr-OL in layer 2, whereas the BC-UO and the BC-LO in layer 2 as well as the Zmj and the PL should be passively extended, and the DAO in layer 1 and the MN should be tensed statically (Case 8, Fig. 6h). (Table 2)

4. What we can learn from the new scheme of perioral muscle architecture

We proposed a unique scheme for the architecture of the perioral muscle based on the study of isolated muscle specimens. This scheme was different from the conventional views of their architecture at several points, and could provide a new functional relevance of the actions of these muscles.

In the first place, we revealed that the SOOr-IM and the IOOr-IM were structurally distinct and functionally different from the SOOr-OL and the IOOr-OL. The fascicles of the SOOr-IM and the IOOr-IM were continuous with the BC-MT and arose from the pterygomandibular raphe. Thus the SOOr-IM and the IOOr-IM are able to close the oral fissure lightly, whereas the SOOr-OL and the IOOr-OL arose from the modiolus, and would impose upon both lips to deform them.

The second point concerned the connection of the SOOr-OL with the other perioral muscles. Our findings revealed that the SOOr-OL was connected with the DAO in the vertical direction, and did not connect with the BC as previously supposed. Thus the SOOr-OL together with the DAO could pull the modiolus upward (elevation) or downward (depression) as well as medially (adduction), and as a whole depress the whole upper lip downward to close the oral fissure.

The third point concerned the coupling of the IOOr-OL with the BC in the horizontal direction and its mixed population of fascicles. We revealed that the fascicles of the IOOr-OL were either continuous directly with the BC-MT or connected indirectly with the BC-UO and the BC-LO at the modiolus. Thus the IOOr-OL together with the BC-UO and the BC-LO could pull the modiolus laterally (abduction) or medially (adduction) depending on the relative strength of tension and as a whole elevate the oral fissure to close it.

Taken together the findings of the present study clarified the architecture of the perioral muscles around the central hub of modiolus as a unified functional system, and made it possible to specify the function of individual component muscles within the system. It also became evident that the upper lip and the lower lip with the SOOr and the IOOr as the active functional components were neither symmetrical vertically nor equivalent, in contrast to the classical view of the OOr in previous anatomy studies and textbooks hypothesizing the vertical symmetry and similarity between the upper and the lower lips [20, 24].

buccinator

BC-LO

lower oblique part of BC

BC-LT

lowest transverse part of the BC

BC-MT

middle transverse part of BC

BC-UO

upper oblique part of BC

DAO

depressor anguli oris

DLI

depressor labii inferioris

ILI

incisivus labii inferioris

ILS

incisivus labii superioris

IOOr

inferior OOr

IOOr-IM

inner marginal part of IOOr

IOOr-OL

outer labial part of IOOr

LAO

levator anguli oris

LLS

levator labii superioris

mentalis

OOr

orbicularis oris

platysma

SOOr

superior OOr

SOOr-IM

inner marginal part of SOOr

SOOr-OL

outer labial part of SOOr

Zmj

zygomaticus major

Funding

The authors did not receive support from any organization for the submitted work.

Ethics approval

Author contributions

Conceptualization, MI and TS; cadaver preparation, KI and KK; data curation, MI, KK and TS; data validation, KK and TS; and manuscript writing, MI and TS.

Acknowledgements

The authors thank the individuals who donated their bodies to Juntendo University School of Medicine so the anatomical research could be performed. Results from such research can potentially increase mankind’s overall knowledge that can them improve patient care. Therefore, those donors and their families deserve our highest gratitude.

Conflict of interest

The authors declare no potential conflict of interest.

Data availability

On reasonable request, the obtained data supporting the finding of the present study are available from the corresponding authors.

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Table 1. Structure and function of the three layers of perioral muscles.

Layer 1

Structure: DAO = [modiolus] = SOOr-OL

Function: 1) Depression and deformation of the upper lip. 2) Adduction of the modiolus. 3) Elevation or depression of modiolus, depending on the relative strength of DAO and SOOr.

Layer 2

Structure: BC-UO, BC-LO = [modiolus] = IOOr-OL, with ILI

Function: 1) Elevation and deformation of the lower lip. 2) Adduction or abduction of the modiouls, depending on the relative strength of BC and IOOr.

Layer 3

Structure: BC-MT = SOOr-IM + IOOr-IM + IOOr-OL (lower bundle)

Function: 1) Lowering the upper lip margin. 2) Raising the lower lip margin.

No competing interests reported.

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Orbicularis oris and buccinator as a sphincter complex of the oral fissure – re-evaluation using isolated muscle specimens.

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