Introduction

The facial muscles are mainly composed of the muscles of facial expression, also called the mimetic muscles. The orbicularis oculi muscle is representative of the mimetic muscles; it has been frequently reported in relation to plastic surgery owing to the important role of movement production around the orbital region in manifesting several emotions (Hamra 1992; Besins 2004; Most et al. 2005; Spiegel and DeRosa 2005; Carriquiry et al. 2006; Alghoul and Codner 2013). Other reports have discussed the orbicularis oculi muscle as it relates to the appearance of facial aging (Furnas 1978; Fogli 1992; Pottier et al. 2008).

In general, the orbicularis oculi muscle has been considered to consist of three parts: the orbital, palpebral, and lacrimal parts surrounding the orbit (Standring 2015). The studies cited above focused mainly on the orbital part of the orbicularis oculi muscle (Oo), as it is the part that is strongly related to the appearance of facial aging (Furnas 1978; Fogli 1992; Pottier et al. 2008) or facial rejuvenation (Hamra 1992; Besins 2004; Most et al. 2005; Spiegel and DeRosa 2005; Carriquiry et al. 2006; Alghoul and Codner 2013). The Oo is generally described as surrounding the palpebral part of the orbicularis oculi muscle, which spreads its fibers across the eyelids (Standring 2015). The Oo arises from the nasal process of the frontal bone, the frontal process of the maxilla, and the medial palpebral ligament (Standring 2015). It is also generally accepted that its outermost muscle fibers usually extend to adjoin with the muscles of the periorbital regions, especially in the region inferior to the Oo (Most et al. 2005; Spiegel and DeRosa 2005; Flint et al. 2010; Standring 2015).

In the region inferior to the Oo, the proper midfacial muscles such as the zygomaticus minor (ZMi), the zygomaticus major (ZMj), the levator labii superioris alaeque nasi (LLSAN), and the levator labii superioris (LLS) muscles are observed. The distinct muscle bundles found in this region were first described by Henle (1858), who named these muscle bundles the malaris muscle. Henle (1858) described the malaris muscle as being composed of medial and lateral parts. Lightoller (1925) also stated that these muscle bundles are the medial and lateral heads of the malaris muscle. In the present study, we use the terms “medial and lateral bundles” in reference to the medial and lateral parts in the study of Henle (1858) as well as the medial and lateral heads in the study of Lightoller (1925). However, in recent years, some studies have considered the lateral bundles of the malaris muscle originating from the superficial temporal fascia to be an independent group, due to its involvement in midfacial aging (Zufferey 2005, 2013; Park et al. 2011). Hwang et al. (2002) identified the medial bundles as the aberrant muscle of the orbicularis oculi muscle and named them the orbitozygomatic muscle. However, Park et al. (2012) examined these muscle bundles and concluded that they are parts of the orbicularis oculi muscle. Therefore, the medial bundles of the malaris described by Henle (1858) and Lightoller (1925) have not been studied for a long time.

The aim of the present study was to examine in detail the muscle bundles in the region inferior to the Oo that are not the proper midfacial muscles (i.e., not the ZMi, the ZMj, the LLSAN, and the LLS). In this study, the inferior part of the Oo was distinguished from the lateral bundles that attach to the superficial temporal fascia at the lateral margin of the Oo. Moreover, we found lateral bundles running along the inferior margin of the Oo which had attachments in the medial side, in common with the Oo. Such muscle bundles were distinguished from the lateral bundles in this study and were identified as the suspending bundles. The nerves innervating the midfacial muscles were also analyzed in detail to classify the midfacial muscles. In addition, in order to clarify the positional relationships between the suspending bundles and the surrounding tissues, including the Oo, sagittal histological sections were also examined.

Materials and methods

We studied twelve head regions of Japanese cadavers (eight males and four females, age 56–97 years, average age 82.5 years old). The cadavers used in the present study were donated to the Department of Anatomy, Tokyo Medical and Dental University, Japan. The format of the document is congruent with the Japanese law entitled Act on Body Donation for Medical and Dental Education. All of the donors voluntarily declared before their deaths that their remains would be donated as materials for education and study. This voluntary donor system of cadavers is applied throughout Japan, and our study completely complies with the current laws of Japan.

All cadavers were fixed by arterial perfusion with 8% formalin and preserved in 30% alcohol. Ten heads were used for the macroscopic investigation. Two heads were cut in half along the median line. The two left halves of the heads were used for macroscopic investigations, and two right halves of the heads were used for histological investigation.

For the macroscopic investigations, the skin and subcutaneous tissues of all specimens used in this study were removed to examine the facial muscles. The muscles, especially those in the region between the forehead and the upper lip, were carefully dissected to examine the muscle bundles around the Oo, especially additional muscle bundles and variations in them.

After dissecting the facial muscles, three female heads were chosen at random. After cutting the nerves of the trigeminal nerve, the facial muscles and branches of the facial nerve were carefully removed from the skulls en bloc. These specimens were immersed in water and were cautiously dissected from the inner surfaces under an operating microscope to examine the patterns of the innervating branches of the facial nerve.

Histological examinations were performed on the two right halves of the heads (two males). We sagittally sliced these heads at the region of the mid-medial third of the inferior orbital region using a diamond band pathology saw (EXAKT 312; EXAKT Advanced Technologies, Norderstedt, Germany). These specimens were decalcified with Plank–Rychlo solution (AlCl3·6H2O, 126.7 g/l; HCl, 85 ml/l; HCOOH, 50 ml/l) for 4 days and then embedded in paraffin, sliced into 5-μm-thick sections, and stained with Elastica van Gieson stain.

Results

Macroscopic observations of the Oo and the neighboring muscles

The Oo chiefly spread to form an oval shape around the orbit. In all specimens, the muscle fibers of the Oo were observed to typically arise from the nasal process of the frontal bone, the frontal process of the maxilla, and the medial palpebral ligament. Within the region adjacent to the inferior part of the Oo, the midfacial proper muscles, such as the ZMi, the ZMj, the LLS, and the LLSAN, were generally observed. The ZMi and ZMj were found to arise from the zygomatic bone. In addition, the LLSAN was found to originate from the superior part of the frontal process of the maxilla, and the LLS from the maxilla and zygomatic bone.

During the dissection procedures, extra muscle bundles were constantly observed in the region inferior to the Oo. These extra muscle bundles were identified and classified into lateral, medial, and suspending bundles inferior to the Oo (Fig. 1). The lateral and suspending bundles were found in all specimens, whereas the medial bundles were noted in only 9 of 22 specimens (40.9%). Detailed descriptions of the lateral, medial, and the suspending bundles are given below.

Fig. 1
figure 1

The extra muscle bundles in the region inferior to the Oo, composed of lateral (LB), medial (MB), and suspending (SB) bundles. Dotted lines indicate the region of the eyelid. FB frontal belly of occipitofrontalis muscle, Oo orbital part of orbicularis oculi muscle, LLSAN levator labii superioris alaeque nasi muscle, LLS levator labii superioris muscle, ZMi zygomaticus minor muscle, ZMj zygomaticus major muscle

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The lateral bundles were observed in all specimens. These lateral bundles clearly arose from the lateral surface of the superficial temporal fascia then ran inferiorward and adjoined with ZMi in all specimens (Fig. 2a) and with ZMj in 14 of 22 specimens (63.6%, Fig. 2b). Some muscle bundles were observed to run inferiorly towards the platysma muscles in 8 of 22 specimens (36.4%, Fig. 2a).

Fig. 2
figure 2

Attachments of the lateral bundles. a LB1 represents the lateral bundles that blended with the zygomaticus minor muscle (ZMi). LB3 represents the lateral bundles that extending towards the platysma muscle (Pla). b LB2 represents the lateral bundles that blended with the zygomaticus major muscles (ZMj). SB suspending bundle, Oo orbital part of orbicularis oculi muscle, LLSAN levator labii superioris alaeque nasi muscle, LLS levator labii superioris muscle

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The medial bundles were noticed in 9 of 22 specimens (40.9%). These medial bundles ran inferiorly and adjoined with the LLSAN and/or the LLS (Fig. 3a). The medial bundles from the frontal process of the maxilla and from the medial palpebral ligament were observed in 4 of 9 specimens (44.4%) and in 4 of 9 specimens (44.4%), respectively. Furthermore, some medial bundles were found to run across the medial palpebral ligament and to connect with the frontal belly of the occipitofrontalis (FB) in 7 of 9 specimens (77.8%). Moreover, it was interestingly to observe that the medial bundles were adjoined only to the FB in 2 of 9 specimens (22.2%, Fig. 3b).

Fig. 3a–b
figure 3

Attachments of the medial bundles. a The medial bundles (MB) blended with the levator labii superioris alaeque nasi (LLSAN) and/or the levator labii superioris (LLS) muscles. b The medial bundles (MB) ran across the medial palpebral ligament and adjoined with the frontal belly of the occipitofrontalis (FB). Oo orbital part of orbicularis oculi muscle, ZMi zygomaticus minor muscle, ZMj zygomaticus major muscle, SB suspending bundle

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In the present study, a U-shaped muscle bundle adjacent to the inferior border of the Oo was observed in all of the specimens; we termed this “the suspending bundle” in order to simplify notation. The lateral attachment of the suspending bundle was derived from the superficial temporal fascia in all specimens. On the medial side, there was frequently a deep groove between the suspending bundle and the Oo, particularly in the medial half of the orbit when there was anterior protrusion of the inferior orbital fat. Consequently, the suspending bundle and the Oo could be distinguished by the lateral attachments and the medial groove. The medial attachments of the suspending bundles were derived from the frontal process of the maxilla in all specimens (Fig. 4a) and the medial palpebral ligament in 15 of 22 specimens (68.2%, Fig. 4b). Regarding the medial bundles, as previously described, the suspending bundles also adjoined with the FB in 15 of 22 specimens (68.2%, Fig. 4c). In addition, it was interesting to observe that the suspending bundle was frequently sparse and interrupted (Figs. 1, 2, 3, and 4a, b).

Fig. 4
figure 4

The attachments of the suspending bundles. The suspending bundles (SB) were derived from the medial attachments, consisting of the frontal process of the maxilla (a; FPoM) and the medial palpebral ligament (b; MPL), and they crossed over the MPL to attach to the frontal belly of the occipitofrontalis muscle (c; FB). In contrast, the lateral attachment was derived from the superficial temporal fascia. Oo orbital part of orbicularis oculi muscle, LLSAN levator labii superioris alaeque nasi muscle, LLS levator labii superioris muscle, ZMi zygomaticus minor muscle, ZMj zygomaticus major muscle

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Innervation patterns of the Oo and the neighboring muscles

The innervation patterns of the orbicularis oculi muscle and the neighboring muscles were carefully examined. After passing through the parotid gland, several branches of the facial nerve were identified and classified as temporal and zygomatic branches according to their distributions (Fig. 5). The temporal branches ran superomedially to innervate the lateral part of the orbicularis oculi muscle, and the zygomatic branches ran medially to innervate the medial part of the muscle (Fig. 5). Some of the temporal branches ran superiorly to innervate the lateral bundles and the lateral parts of the suspending bundle and the Oo (Fig. 5a, c). It was noted that a few branches innervating the lateral bundles passed through the bundles to innervate the suspending bundle and the Oo (Fig. 5b).

Fig. 5
figure 5

Innervation patterns of the branches of the facial nerve. a Dashed box indicates the region of shown in b. b Courses of the temporal branches (green arrowheads). c Red box indicates the region shown in d. d Courses of the zygomatic branches (blue arrowheads). Oo orbital part of orbicularis oculi muscle, ZMi zygomaticus minor muscle, ZMj zygomaticus major muscle, LLSAN levator labii superioris alaeque nasi muscle, SB suspending bundle, LB lateral bundles

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Most of the zygomatic branches ran medially to innervate the midfacial proper muscles (including LLSAN, LLS, ZMi, and ZMj) from their inner surfaces. Some of these branches penetrated their muscles to innervate the medial bundles and the suspending bundle, and a few of these branches then penetrated the suspending bundle again to innervate the medial part of the Oo (Fig. 5d).

Histological observations of the sagittal sections of the middle part of the orbital region

As previously described, a deep groove between the Oo and the suspending bundle on the medial side of the orbital region was frequently observed (Fig. 6a). In order to clarify the positional relationships of the suspending bundles to the surrounding tissues, including the Oo, sagittal histological sections were obtained at the position of the medial one-third (Fig. 6b). At this position, the intraorbital fat tissue was protruding anteriorly, and the suspending bundle was observed inferior to the orbital septum (Fig. 6c, d). In these sections, although the Oo was thin and weak, the suspending bundle was relatively thick. In one specimen, the cheek fatty tissue was protruding superiorly, and the superior end of the fatty tissue was situated between the suspending bundle and the inferior margin of the orbit of the maxilla.

Fig. 6
figure 6

Histological observations of the sagittal sections of the middle part of the orbital region. a Deep groove between the Oo and the suspending bundle (SB). b Orange line indicates the cutting section. c and d Relationship between the SB and the intraorbital fat (IOF); blue dot indicates the superior protrusion of the fat tissue to the orbital septum (OS). Oo orbital part of orbicularis oculi muscle, LLS levator labii superioris muscle

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Discussion

The present study revealed extra muscle bundles located in the region between the inferior margin of the Oo and the proper midfacial muscles (including ZMi, ZMj, LLSAN, and LLS; Fig. 7). Henle (1858) and Lightoller (1925) reported that the medial and lateral bundles of the malaris muscle are observed within this region. However, since then, these two muscle bundles of the malaris muscle have not been described together in the same study. Interestingly, a suspending bundle adjacent to the inferior part of the Oo in the present study was observed in all specimens. The lateral bundles observed in this study should perhaps be considered a muscle that is independent of the Oo, in accordance with previous reports (Henle 1858; Lightoller 1925; Zufferey 2005, 2013; Park et al. 2011). In addition, regardless of the name assigned to them, the medial bundles observed in this study could be regarded as the same muscle bundle as the orbitozygomatic muscle (Hwang et al. 2002), and parts of the orbicularis oculi muscle (Park et al. (2012), including the medial bundle of the malaris muscle (Henle 1858; Lightoller 1925). Since the suspending bundle in this study ran between the attachments of the medial and lateral bundles, not only the lateral and medial bundles but also the suspending bundle found in this study can be regarded as the same muscle complex consisting of the malaris muscle.

Fig. 7
figure 7

Illustration of the relationship of the extra muscle bundles to the neighboring muscle. FB frontal belly of occipitofrontalis muscle, Oo orbital part of orbicularis oculi muscle, LLSAN levator labii superioris alaeque nasi muscle, LLS levator labii superioris muscle, ZMi zygomaticus minor muscle, ZMj zygomaticus major muscle, LB lateral bundles, SB suspending bundle, MB medial bundles

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The Oo and the malaris muscle comprising the lateral, medial, and suspending bundles were apparently innervated by the temporal and zygomatic branches of the facial nerve. Through the courses of these branches, we noted that a few of the temporal branches penetrated the lateral bundles from the inner to the outer aspects and then innervated the suspending bundle and the lateral part of the Oo. Similarly, a few of the zygomatic branches also penetrated ZMj, ZMi, and the suspending bundle to innervate the medial part of the Oo. Most of previous reports described the facial expression muscles as being arranged from deep to superficial layers (Ouattara et al. 2004; Turvey and Golden 2012; Mendelson and Wong 2013; Marur et al. 2014; Roostaeian et al. 2015). Moreover, in some previous reports, the Oo and ZMi were considered to belong to the most superficial layer of facial expression muscles, whereas ZMj, LLS, and LLSAN were regarded as deeper muscles than the Oo (Freilinger et al. 1987; Spiegel and DeRosa 2005; reviewed by Christensen et al. 2016). Based on the innervation patterns recognized in this study, the muscle bundles in the region between the inferior margin of the Oo and the proper midfacial muscles (including ZMi, ZMj, LLSAN, and LLS) may be considered to have a stepwise arrangement. In other words, the muscle bundles of the malaris muscle can be classified as a deep facial muscle in comparison with the Oo, or as a superficial facial muscle in comparison with the proper midfacial muscles. Therefore, the muscle bundles of the malaris muscle may occupy the transitional layer between the superficial and deep facial muscles. In addition, although the ZMi and Oo are reported to be located in the same superficial layer according to previous studies (Freilinger et al. 1987; Spiegel and DeRosa 2005; reviewed by Christensen et al. 2016), the ZMi seemed to be a deeper muscle than the Oo in this study. This may be because ZMi could not be clearly distinguished from the lateral bundles of the malaris muscle.

It has been reported that the orbicularis oculi muscle becomes atrophic, stretched, or thin with age, and this thinness and weakness of the muscle could lead to the herniation of the orbital fat (del Campo 2008; Okuda et al. 2012a, b). Such a protrusion of the intraorbital fat is also reportedly caused by various factors, including orbital fat prolapse, loss of skin elasticity, as well as laxity of the orbicularis oculi muscle (Furnas 1978; Goldberg et al. 2005; Okuda et al. 2012a). The histological sections obtained in the present study (Fig. 6) suggested that the Oo becomes thinner than the other muscle structures, whereas the suspending bundle found in the present study seemed to be thicker than the Oo. Based on the positional relationships between the suspending bundle and the intraorbital structures, the role of the suspending bundle could be to sustain the intraorbital structures. The medial end of the suspending bundle mainly attaches to the bony elements on the medial side, and the lateral end attaches to the superficial temporal fascia. For this reason, strong forces could act more easily at the medial end than at the lateral end, and the lateral end may then descend due to the apparent volume loss of the temporal fossa with aging (Juhász and Marmur 2015). At the inferolateral side of the suspending bundle, the laxity of the muscle bundle could cause them to droop, creating a space in which fatty tissues appear (Park et al. 2012). This may be why the deep groove between the Oo and the suspending bundle in particular was frequently observed, especially on the medial side. Such a groove could be generated between the thin Oo and the thick suspending bundle, and the herniation of the orbital fat would make the groove more obvious, especially on the medial side.

In conclusion, the malaris muscle is a muscle group that is situated inferior to the Oo and consists of three muscle bundles. Based on the local morphology and innervation patterns, this muscle group corresponds to a muscle that is independent of the orbicularis oculi muscle, and should be considered a transitional muscle group between the Oo and the midfacial proper muscle group (including ZMj, Zmi, LLS, and LLSAN). The malaris, especially the suspending bundle adjacent to the inferior part of the Oo, is considered to play a role in sustaining the intraorbital structures, and could generate the obvious groove between the suspending bundle and the Oo through the herniation of the intraorbital fat tissues with aging.