Evolution of the Muscles of Facial Expression in a Monogamous Ape: Evaluating the Relative Influences of Ecological and Phylogenetic Factors in Hylobatids

Facial expression is a communication mode produced by facial (mimetic) musculature. Hylobatids (gibbons and siamangs) have a poorly documented facial display repertoire and little is known about their facial musculature. These lesser apes represent an opportunity to test hypotheses related to the evolution of primate facial musculature as they are the only hominoid with a monogamous social structure, and thus live in very small groups. Primate species living in large groups with numerous social relationships, such as chimpanzees and rhesus macaques, have been shown to have a complex facial display repertoire and a high number of discrete facial muscles. The present study was designed to examine the relative influence of social structure and phylogeny on facial musculature evolution by comparing facial musculature complexity among hylobatids, chimpanzees, and rhesus macaques. Four faces were dissected from four hylobatid species. Morphology, attachments, three‐dimensional relationships, and variation among specimens were noted and compared to rhesus macaques and chimpanzees. Microanatomical characteristics of the orbicularis oris muscle were also compared. Facial muscles of hylobatids were generally gracile and less complex than both the rhesus macaque and chimpanzee. Microanatomically, the orbicularis oris muscle of hylobatids was relatively loosely packed with muscle fibers. These results indicate that environmental and social factors may have been important in determining morphology and complexity of facial musculature in the less social hylobatids and that they may not have experienced as strong selection pressure for mimetic muscle complexity as other, more social primates. Anat Rec, 294:645–663, 2011. © 2011 Wiley‐Liss, Inc.     

A functional and clinical reinterpretation of human perineal neuromuscular anatomy: Application to sexual function and continence

Modern anatomical and surgical references illustrate perineal muscles all innervated by branches of the pudendal nerve but still organized into anatomically distinct urogenital and anal triangles with muscles inserting onto a central perineal body. However, these conflict with the anatomy commonly encountered during dissection. We used dissections of 43 human cadavers to characterize the anatomical organization of the human perineum and compare our findings to standard references. We found bulbospongiosus and the superficial portion of the external anal sphincter (EAS) were continuous anatomically with a common innervation in 92.3% of specimens. The superficial transverse perineal muscle inserted anterior and lateral to the midline, interdigitating with bulbospongiosus. The three EAS subdivisions were anatomically discontinuous. Additionally, in 89.2% of our sample the inferior rectal nerve emerged as a branch of S3 and S4 distinct from the pudendal nerve and innervated only the subcutaneous EAS. Branches of the perineal nerve innervated bulbospongiosus and the superficial EAS and nerve to levator ani innervated the deep EAS. In conclusion, we empirically demonstrate important and clinically relevant differences with perineal anatomy commonly described in standard texts. First, independent innervation to the three portions of EAS suggests the potential for functional independence. Second, neuromuscular continuity between bulbospongiosus and superficial EAS suggests the possibility of shared or overlapping function of the urogenital and anal triangles. Clin. Anat. 29:1053–1058, 2016. © 2016 Wiley Periodicals, Inc.     

Morphological Features of the Branching Pattern of the Hypoglossal Nerve

The hypoglossal or twelfth cranial nerve is the motor nerve to the extrinsic and intrinsic muscles of the tongue, and the superior root of the ansa cervicalis and the thyrohyoid and geniohyoid branches are delivered through the nerve. This study investigated the muscular branches of the hypoglossal nerve to clarify their spatial relationships with the muscles of the tongue and the neighboring structures. The muscles and the nerve were gross anatomically examined in 42 cadavers. The superior root and the thyrohyoid branch left the nerve near the occipital and lingual arteries, respectively. The extrinsic muscles consisted of some components, and the geniohyoid branch and the lingual branches arose on the hyoglossus. The ascending lingual branches formed a plexus on the anterior part of the hyoglossus and were divided into the proximal and distal groups. They supplied the two parts of the hyoglossus, the three bundles of the styloglossus and the superior and inferior longitudinal muscles and communicated with the lingual nerve. The descending lingual branches supplied the inferior part of the genioglossus, and the terminal branches gave intramuscular twigs to its main part and the transverse and vertical muscles. The findings indicated that the branching pattern of the hypoglossal nerve is characterized by the positional relationships to the components of the extrinsic muscles. The hyoid bone can be an effective marker to identify the branches and affected position if it was used in combination with the morphology of the extrinsic muscles, and the knowledge of their variations is also beneficial. Anat Rec, 302:558–567, 2019. © 2018 Wiley Periodicals, Inc.     

Manual stimulation of the whisker pad after hypoglossal–facial anastomosis (HFA) using a Y-tube conduit does not improve recovery of whisking function

Facial nerve injury is a common clinical trauma involving long-term functional deficits with facial asymmetry leading to associated psychological issues and social hardship. We have recently shown that repair by hypoglossal–facial or facial–facial nerve surgical end-to-end anastomosis and suture [hypoglossal–facial anastomosis (HFA) or facial–facial anastomosis (FFA)] results in collateral axonal branching, polyinnervation of neuromuscular junctions (NMJs) and poor function. We have also shown that another HFA repair procedure using an isogenic Y-tube (HFA + Y-tube) and involving a 10-mm gap reduces collateral axonal branching, but fails to reduce polyinnervation. Furthermore, we have previously demonstrated that manual stimulation (MS) of facial muscles after FFA or HFA reduces polyinnervation of NMJs and improves functional recovery. Here, we examined whether HFA + Y-tube and MS of the vibrissal muscles reduce polyinnervation and restore function. Isogenic Y-tubes were created using abdominal aortas. The proximal hypoglossal nerve was inserted into the long arm and sutured to its wall. The distal zygomatic and buccal facial nerve branches were inserted into the two short arms and likewise sutured to their walls. Manual stimulation involved gentle stroking of the vibrissal muscles by hand mimicking normal whisker movement. We evaluated vibrissal motor performance using video-based motion analysis, degree of collateral axonal branching using double retrograde labeling and the quality of NMJ reinnervation in target musculature using immunohistochemistry. MS after HFA + Y-tube reduced neither collateral branching, nor NMJ polyinnervation. Accordingly, it did not improve recovery of function. We conclude that application of MS after hypoglossal–facial nerve repair using an isogenic Y-tube is contraindicated: it does not lead to functional recovery but, rather, worsens it.     

Of Mice,Monkeys, And Men: Physiological And Morphological Evidence For Evolutionary Divergence Of Function In Mimetic Musculature

Facial expression is a universal means of visual communication in humans and many other primates. Humans have the most complex facial display repertoire among primates; however, gross morphological studies have not found greater complexity in human mimetic musculature. This study examines the microanatomical aspects of mimetic musculature to test the hypotheses related to human mimetic musculature physiology, function, and evolutionary morphology. Samples from the orbicularis oris muscle (OOM) and the zygomaticus major (ZM) muscle in laboratory mice (N = 3), rhesus macaques (N = 3), and humans (N = 3) were collected. Fiber type proportions (slow‐twitch and fast‐twitch), fiber cross‐sectional area, diameter, and length were calculated, and means were statistically compared among groups. Results showed that macaques had the greatest percentage of fast fibers in both muscles (followed by humans) and that humans had the greatest percentage of slow fibers in both muscles. Macaques and humans typically did not differ from one another in morphometrics except for fiber length where humans had longer fibers. Although sample sizes are low, results from this study may indicate that the rhesus macaque OOM and ZM muscle are specialized primarily to assist with maintenance of the rigid dominance hierarchy via rapid facial displays of submission and aggression, whereas human musculature may have evolved not only under pressure to work in facial expressions but also in development of speech. Anat Rec, 297:1250–1261, 2014. © 2014 Wiley Periodicals, Inc.     

Anatomical study of the zygomatic and buccal branches of the facial nerve: Application to facial reanimation procedures

The facial nerve is responsible for any facial expression channeling human emotions. Facial paralysis causes asymmetry, lagophthalmus, oral incontinence, and social limitations. Facial dynamics may be re‐established with cross‐face‐nerve‐grafts (CFNG). Our aim was to reappraise the zygomaticobuccal branch system relevant for facial reanimation surgery with respect to anastomoses and crossings. Dissection was performed on 106 facial halves of 53 fresh frozen cadavers. Study endpoints were quantity and relative thickness of branches, correlation to “Zuker's point”, interconnection patterns and crossings. Level I and level II branches were classified as relevant for CFNG. Anastomoses and fusion patterns were assessed in both levels. The zygomatic branch showed 2.98 ± 0.86 (range 2–5) twigs at level II and the buccal branch 3.45 ± 0.96 (range 2–5), respectively. In the zygomatic system a single dominant branch was present in 50%, two co‐dominant branches in 9% and three in 1%. In 66% of cases a single dominant buccal twig, two co‐dominant in 12.6%, and three in 1% of cases were detected. The most inferior zygomatic branch was the most dominant branch (P = 0.003). Using Zuker's point, a facial nerve branch was found within 5 mm in all facial halves. Fusions were detected in 80% of specimens. Two different types of fusion patterns could be identified. Undercrossing of branches was found in 24% at levels I and II. Our study describes facial nerve branch systems relevant for facial reanimation surgery in a three‐dimensional relationship of branches to each other. Clin. Anat. 32:480–488, 2019. © 2019 Wiley Periodicals, Inc.     

Distal variations of the neurovascular pedicle of the serratus anterior muscle as a flap

The serratus anterior muscle has recently been suggested as a versatile and reliable flap for reconstruction of complex craniofacial and neck lesions, extremity and sacroiliac region injuries, as well as intrathoracic and extrathoracic reconstruction procedures. The muscle has been used as a microvascular flap or a pedicled transfer and has been transferred in combination with other muscles, bones, and skin. We performed 15 dissections of adult axilla regions that were examined under ×3.5 loupe magnification to collect anatomic data regarding the neurovascular pedicle of the serratus anterior muscle. The serratus muscle and fascia were found to have a dual blood supply, with the upper part supplied by the lateral thoracic artery and the lower part by terminal branches of the thoracodorsal artery. The lateral thoracic artery was noted to supply the upper four slips but it extended into the lower serratus anterior muscle in two cases. Seven branching patterns were found in the lower serratus anterior muscle. In type I, the only branch of serrati proceeded over the long thoracic nerve. Type II had the only branch of serrati proceeding under the long thoracic nerve. In type III, double branches of serrati proceeded over the long thoracic nerve; while in type IV branches of serrati ran with a double branch under the long thoracic nerve. In type V, three serrati branches proceeded over the long thoracic nerve. Type VI serrati branches were branches of thoracodorsalis, which was hypoplastic, and the supply was maintained from the lateral thoracic artery. In type VII, one serrati branch ran over the long thoracic nerve. There was no connection between the branches of serrati and the branches of the lateral thoracic artery. The length of the long thoracic nerve, the number of motor axons and the vascular network in anatomic proximity to this nerve make it an expendable but powerful source of reconstructions of head, neck, chest wall and extremity defects. Results of this study provide an anatomic framework to improve current reconstructive or aesthetic procedures on the serratus anterior neurovascular structures.     

Intralaryngeal neuroanatomy of the recurrent laryngeal nerve of the rabbit

We undertook this study to determine the detailed neuroanatomy of the terminal branches of the recurrent laryngeal nerve (RLN) in the rabbit to facilitate future neurophysiological recordings from identified branches of this nerve. The whole larynx was isolated post mortem in 17 adult New Zealand White rabbits and prepared using a modified Sihler's technique, which stains axons and renders other tissues transparent so that nerve branches can be seen in whole mount preparations. Of the 34 hemi-laryngeal preparations processed, 28 stained well and these were dissected and used to characterize the neuroanatomy of the RLN. In most cases (23/28) the posterior cricoarytenoid muscle (PCA) was supplied by a single branch arising from the RLN, though in five PCA specimens there were two or three separate branches to the PCA. The interarytenoid muscle (IA) was supplied by two parallel filaments arising from the main trunk of the RLN rostral to the branch(es) to the PCA. The lateral cricoarytenoid muscle (LCA) commonly received innervation from two fine twigs branching from the RLN main trunk and travelling laterally towards the LCA. The remaining fibres of the RLN innervated the thyroarytenoid muscle (TA) and comprised two distinct branches, one supplying the pars vocalis and the other branching extensively to supply the remainder of the TA. No communicating anastomosis between the RLN and superior laryngeal nerve within the larynx was found. Our results suggest it is feasible to make electrophysiological recordings from identified terminal branches of the RLN supplying laryngeal adductor muscles separate from the branch or branches to the PCA. However, the very small size of the motor nerves to the IA and LCA suggests that it would be very difficult to record selectively from the nerve supply to individual laryngeal adductor muscles.     

Lateromedial and dorsoplantar borders among supplying areas of the nerves innervating the intrinsic muscles of the foot

The branching patterns of nerves supplying the intrinsic muscles of the foot were analyzed as a basis to confirm the muscle layer structure. Thirty‐eight feet of 20 Japanese cadavers were examined in detail in this study. The first dorsal interosseus was innervated by a branch from the deep peroneal nerve as well as a branch of the lateral plantar nerve in 92.1%, the second dorsal interosseus in 10.5% and the third dorsal interosseus in 2.6%. In three specimens, branches from the deep peroneal nerve innervated the oblique head of the adductor hallucis or the lateral head the flexor hallucis brevis. In addition, branches from the medial and lateral plantar nerves and the deep peroneal nerve formed communication loops in three specimens. The first dorsal interosseus, the oblique head of the adductor hallucis and the lateral head of the flexor hallucis and their innervating nerve branches are closely related within the first intermetatarsal space. Since the tibial part of the first interosseus muscle primordium is occupied in the space during development, the variations of innervation patterns and formation of the communicating nerve loops may be explained by various combinations of the part and the other muscle primordia. Anat Rec 255:465–470, 1999. © 1999 Wiley‐Liss, Inc.     

The Muscular Branching Patterns of the Ulnar Nerve to the Flexor Carpi Ulnaris and Flexor Digitorum Profundus Muscles

The branching pattern of the ulnar nerve in the forearm is of great importance in anterior transposition of the ulnar nerve for decompression after neuropathy of cubital tunnel syndrom and malformations resulting from distal end fractures of the humerus. In this study, 37 formalin-fixed forearms were used to demonstrate the muscular branching patterns from the main ulnar nerve to the flexor carpi ulnaris muscle (FCU) and ulnar part of the flexor digitorum profundus muscle (FDP). Eight branching patterns were found and classified into four groups according to the number of the muscular branches leaving the main ulnar nerve. Two (Group I) and three (Group II) branches left the main ulnar nerve in 18 and 17 forearms respectively. The remaining two specimens had four (Group III) and five (Group IV) branches each. Usually one or two branches were associated with the innervation of the FCU. However, in 2 cases, three and in one, four branches to FCU were observed. The FDP received a single branch in all cases, except in four, all of which had two branches. In six forearms, a common trunk was observed arising from the ulnar nerve to supply the FCU and FDP. The distribution of the muscular branches to the revealed muscles was outlined in figures and the distance of the origin of these branches from the interepicondylar line was measured in millimeters. The first muscular branch leaving the main ulnar nerve was the FCU-branch in all specimens. The terminal muscular branch of the ulnar nerve to the forearm muscles arose at the proximal 1/3 of the forearm in all specimens. In 7 forearms, Martin-Gruber anastomosis in form of median to ulnar was observed.     

A new method for tracing the facial nerve trunk using the posterior auricular nerve

Tracing the facial nerve trunk is an essential action in parotid surgery, because of the implications of injury to the nerve or its branches. More than a few landmarks that may help the surgeon in this task have been proposed (e.g., the posterior belly of the digastric muscle, the tragal pointer, among others), under the assumption that additional access methods improve the surgical technique and reduce the possibility of harmful post‐operative consequences. Here we present evidence that the posterior auricular nerve may be used to trace the facial nerve trunk. We dissected 75 cadaveric heminecks, exposed the auricularis posterior muscle and adnexa, and attempted to follow the posterior auricular nerve to the facial nerve trunk. The auricularis posterior muscle, nerve, and artery were identified in all heminecks, securing an anatomically reliable route to the facial nerve trunk. Average length of the nerve from the auricularis posterior muscle to the facial nerve trunk was 28 mm (±6.2 mm). The angle between the posterior auricular nerve and the vertical segment of the FN trunk was 39.5° (±7.7°). We conclude that the posterior auricular nerve may be used as a landmark to trace the facial nerve trunk. It is advantageous due to the relatively simple and consistent regional anatomy, and also because manipulation of this nerve does not present a risk given that the auricularis posterior muscle is vestigial. The proposed landmark is particularly important in revision surgery, where the pre‐auricular anatomy may have been distorted and scarred by previous operations. Clin. Anat. 32:453–457, 2019. © 2019 Wiley Periodicals, Inc.     

The malaris muscle: its morphological significance for sustaining the intraorbital structures

The orbicularis oculi muscle, an important mimetic muscle, was investigated to ascertain its anatomical relation to facial aging—especially its orbital part (Oo). Previous studies of the distinct muscle bundles frequently found inferior to the Oo have provided various definitions, including that of the malaris muscle. This study aimed to examine these muscle bundles and clarify their function in facial aging. Twelve heads of Japanese cadavers (average age: 82.5 years old) were dissected to observe the muscles, focusing in particular on those in the periorbital region. Six specimens were further dissected from the inner surfaces to examine the patterns of facial nerve branches under the operating microscope. Histological examinations of two head halves were carried out to investigate the relationship between the muscle bundles and the intraorbital structures. Muscle bundles consisting of lateral, medial, and U-shaped suspending bundles were observed in the region inferior to the Oo. Lateral and suspending bundles were found in all specimens, while the medial bundles were noted in only 9 of 22 specimens. Some branches of the facial nerve penetrated through the lateral, medial, and suspending bundles. The relationship between the suspending bundles and the protruding orbital fat was assessed. The muscle bundles found in this study were regarded as the malaris muscle—a transitional muscle between the superficial and deep facial layers. The suspending bundle may play a role in sustaining the intraorbital structures.     

Main trajectories of nerves that traverse and surround the tympanic cavity in the rat

To guide surgery of nerves that traverse and surround the tympanic cavity in the rat, anatomical illustrations are required that are topographically correct. In this study, maps of this area are presented, extending from the superior cervical ganglion to the otic ganglion. They were derived from observations that were made during dissections using a ventral approach. Major blood vessels, bones, transected muscles of the tongue and neck and supra and infrahyoid muscles serve as landmarks in the illustrations. The course of the mandibular, facial, glossopharyngeal, vagus, accessory and hypoglossal nerves with their branches, and components of the sympathetic system, are shown and discussed with reference to data available in the literature. Discrepancies in this literature can be clarified and new data are presented on the trajectories of several nerves. The course of the tympanic nerve was established. This nerve originates from the glossopharyngeal nerve, enters the tympanic cavity, crosses the promontory, passes the tensor tympani muscle dorsally, and continues its route intracranially to the otic ganglion as the lesser petrosal nerve after intersecting with the greater petrosal nerve. Auricular branches of the glossopharyngeal and of the vagus nerve were noted. We also observed a pterygopalatine branch of the internal carotid nerve, that penetrates the tympanic cavity and courses across the promontory.     

Mimetic Muscles in a Despotic Macaque (Macaca mulatta) Differ from Those in a Closely Related Tolerant Macaque (M. nigra)

Facial displays (or expressions) are a primary means of visual communication among conspecifics in many mammalian orders. Macaques are an ideal model among primates for investigating the co‐evolution of facial musculature, facial displays, and social group size/behavior under the umbrella of “ecomorphology”. While all macaque species share some social behaviors, dietary, and ecological parameters, they display a range of social dominance styles from despotic to tolerant. A previous study found a larger repertoire of facial displays in tolerant macaque species relative to despotic species. The present study was designed to further explore this finding by comparing the gross morphological features of mimetic muscles between the Sulawesi macaque (Macaca nigra), a tolerant species, and the rhesus macaque (M. mulatta), a despotic species. Five adult M. nigra heads were dissected and mimetic musculature was compared to those from M. mulatta. Results showed that there was general similarity in muscle presence/absence between the species as well as muscle form except for musculature around the external ear. M. mulatta had more musculature around the external ear than M. nigra. In addition, M. nigra lacked a zygomaticus minor while M. mulatta is reported to have one. These morphological differences match behavioral observations documenting a limited range of ear movements used by M. nigra during facial displays. Future studies focusing on a wider phylogenetic range of macaques with varying dominance styles may further elucidate the roles of phylogeny, ecology, and social variables in the evolution of mimetic muscles within Macaca Anat Rec, 299:1317–1324, 2016. © 2016 Wiley Periodicals, Inc.     

Masticatory Muscles and Branches of Mandibular Nerve: Positional Relationships Between Various Muscle Bundles and Their Innervating Branches

The masticatory muscles, which are composed of four main muscles, are innervated by branches of only one of the cranial nerves, the mandibular nerve. This muscle group has a variety of very complex functions. We have investigated the origins and insertions of the masticatory muscles and the adjacent bundles of the main muscles, and closely examined the positional relationships between the muscle bundles and innervating branches. According to the findings of the nerve branching patterns, the masticatory muscles can be classified into two groups: the inner group consisting of the lateral pterygoid muscle, and the outer group consisting of the other muscles and adjacent muscle bundles. Further, the outer muscle group is sub-divided into the three other main muscles (the masseter, the temporalis, and the medial pterygoid muscle) and the adjacent various transitional muscle bundles. Anat Rec, 302:609–619, 2019. © 2018 Wiley Periodicals, Inc.     

The long thoracic nerve: Its origin,branches, and relationship to the middle scalene muscle

Anatomical knowledge regarding the long thoracic nerve (LTN) is important during surgical procedures considering that dysfunction of this nerve results in clinical problems. The purpose of this study was to explore the anatomy of the LTN, its origin, configuration, branching pattern, and relationship to the middle scalene muscle (MSM). The course of the LTN was investigated in 12 embalmed cadavers (21 sides). We defined four different types for this nerve according to the origins of its roots. The most common formation of the LTN was the contribution of three branches that originated from the fifth, sixth, and seventh cervical ventral roots. C5 and C6 components or upper portion of the LTN roots lay primarily between the middle and posterior scalene muscles, sometimes passed through the MSM, and less frequently coursed over the MSM. C7 contributions to the LTN were always located anterior to the MSM. Contributions from C8 were also found over the MSM. The median number of branches arising directly from the cervical roots and branches arising from the main trunk of the nerve were 3 and 7, respectively. Along its course, the median number of branches to the serratus anterior was 10. Clin. Anat. 22:476–480, 2009. © 2009 Wiley‐Liss, Inc.     

Surgical anatomy of the radial nerve branches to triceps muscle

The objectives of the study are to demonstrate the innervation patterns of the triceps muscles and the most suitable branch of the radial nerve for nerve transfer to restore the motor function of the deltoid muscle in patients with complete C5–C6 root injury. Seventy‐nine arms (40 left arms and 39 right arms) from 46 embalmed cadavers (24 male and 22 female) were included in the study. The nerves to the triceps were dissected from the triceps muscles (long head, lateral head, and medial head). The lengths of the branches were measured from the main trunk. The distance from the inferior margin of the teres major muscle to the origin of the nerve to the long head, lateral head, and medial head of the triceps were recorded as well. The first branch was the nerve to the long head of the triceps in 79 arms (100%). The second branch was the nerve to the upper medial head in 30 arms (38%), nerve to the medial head in 8 arms (10.1%), nerve to the upper lateral head in 35 arms (44.3%) and nerve to the lateral head in 6 arms (7.6%). The patterns of branches to the triceps were classified according to our dissections. The nerve to the long head of the triceps was constant as the first branch of the nerve to the triceps branch of the radial nerve in the vicinity of the inferior margin of the teres major muscle. Clin. Anat. 2013. © 2012 Wiley Periodicals, Inc.