Development, Structure, and Function of the Zygomatic Bones: What is New and Why Do We Care?

THE ANATOMICAL RECORD 299:1611 1615 (2016) Development, Structure, and Function of the Zygomatic Bones: What is New and Why Do We Care? PAUL C. DECHOW* AND QIAN WANG Department of Biomedical Sciences, Texas A&M University College of Dentistry, Dallas, Texas ABSTRACT This issue of The Anatomical Record is the first of a two-volume set on the zygoma (also called the cheek bone, the zygomatic bone, the malar, or the jugal, the latter term being used in vertebrates other than mammals). The zygoma is an important component of the craniofacial skeleton, in which the zygoma is a connection between the midfacial and the cranial skeletons; has a functional role as the origin of one of the masticatory muscles, the masseter muscle, and several facial muscles; has been considered as an essential buttress of the facial skeleton for resisting masticatory forces; and has importance for determining phylogenetic relationships. In humans, the zygoma is also of aesthetic significance for facial appearance, and its restoration following trauma has resulted in a large clinical literature. In this first volume of this Special Issue, a wide ranging series of papers discuss studies related to issues of development, structure, and function of the zygoma and closely related parts of the craniofacial skeleton in mammals, and in particular primates. This Introductory article provides an overview in which we discuss the primary findings of these studies and some of their implications. The second volume, which will be published as the January 2017 issue of The Anatomical Record, will focus on variation and evolution of the zygoma throughout the vertebrates. Anat Rec, 299:1611 1615, 2016. VC 2016 Wiley Periodicals, Inc. Key words: jugal; craniofacial bones; anatomy; biomechanics; adaptation; evolution; midface This special issue of The Anatomical Record is the first of a two-volume set focused on the cheekbone usually called the zygoma or zygomatic bone (plural: zygomata or zygomatic bones) in mammals, although sometimes referred to as the malar. In reptiles, amphibians, and birds, this bone is called the jugal bone or often just the jugal. This first-volume explores topics related to the development, adaptation, structure, and function of this craniofacial bone primarily in mammals with an emphasis on primates, while the second volume is concerned with its evolution throughout vertebrate history. While difficult to fully separate these topics in the two volumes because most of the studies in the first volume are investigating the zygoma at least in part to shed light on its evolutionary history with concerns relating to evolutionary adaptation, while the second volume looks not only at evolution but also the broad array of forms that this bone has obtained in vertebrates. The latter topic inspired the cover art for these volumes, which illustrates representative vertebrate skulls in a phylogenetic arrangement with the jugal/zygoma highlighted in each case. The left side of the cover art, from bottom to top, are found the sarcopterygian fish Onychodus from Upper *Correspondence to: Dr. Paul C. Dechow, Texas A&M University College of Dentistry, Dallas, TX 75254. Phone: 214-828- 8208 (office) or 469-363-1687 (cell) Email: pdechow@tamhsc.edu Received 19 September 2016; Accepted 19 September 2016. DOI 10.1002/ar.23480 Published online in Wiley Online Library (wileyonlinelibrary. com). VC 2016 WILEY PERIODICALS, INC.

1612 DECHOW AND WANG Devonian of Australia (after Long, 2001), the procolophonid parareptile Kapes from Lower Triassic of Russia (after Novikov and Sues, 2004), the ceratopsid dinosaur Chasmosaurus from Upper Cretaceous of Canada (after Godfrey and Holmes, 1995), and the avian dinosaur Archaeopteryx from Upper Jurassic of Germany (after Elzanowski, 2002). On the right side of the cover art figure, from bottom to top, are found the temnospondyl Dendrerpeton from the Upper Carboniferous of Canada (after Godfrey et al., 1987), the edaphosaurid synapsid Edaphosaurus from Lower Permian of United States of America (after Modesto, 1995), the carnivoran mammal Daphoenus from Oligocene of (after Scott and Jepsen, 1938), and the hominid primate Homo. These drawings are not to scale. The figure is designed by Corwin Sullivan and Xing Xu, and drawn by Yi Liu and Lida Xing of the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences. The broad array of studies found herein is truly amazing when considering the circumscribed nature of this topic. Why the zygoma? What is so interesting about it? In mammals, the zygomata are paired craniofacial bones of great functional importance. Each zygoma connects the facial and cranial bones through sutures and includes articulations with the frontal, maxillary, sphenoid, and temporal bones. The zygomata are the origins for masticatory muscles, in particular the masseter muscles. The bones have interesting variations throughout mammalian and primate evolution that possibly reflect functional adaptations of the midfacial skeleton, and include both cortical and trabecular bone structures. In vivo strain gage studies in select primates have shown an unusual strain gradient in the zygomata, with both high and low magnitudes of strains found in these bones (Ross and Hylander, 1996; Hylander and Johnson, 1997), thus making the zygomata interesting for the study of bone adaptation both during the life of one individual and from an evolutionary perspective. Additionally, in humans, the zygomata are important for aesthetic reasons as the cheekbones form some of the most prominent features of the face. The variations in cortical structure in the human zygoma and in surrounding bones also result in particular patterns of facial fractures that require highly specific protocols for treatment (Ellis et al., 1985). Clinical studies related to a wide of variety of topics such as fracture repair, repair of tissue deficits resulting from the removal of craniofacial tumors, and correction of craniofacial asymmetries make up the vast majority of publications on the zygoma. Here our emphasis is on comparative studies of development, structure, and function and their evolutionary implications. In this article, we will review and place in context the major findings of the articles in this volume. These topics can be divided into two broad categories: (1) development, growth, and adaptation of the zygoma and related bones, and (2) structure and biomechanics of the zygoma, zygomatic arch, and related bones. DEVELOPMENT, GROWTH, AND ADAPTATION OF THE ZYGOMA This volume would be well served to start off with a summary of the evolution and development of the zygoma. This is very well done in the opening sections of the first article (Heuze et al, 2016, this issue). Heuze and colleagues summarize not only the evolutionary history and development of the zygoma but also the historical overlap between these topics in an evodevo approach. The main thrust of their work though is to use a developmental approach that begins to explore the question of the degree of modularity in skull development and how it might be controlled to influence the range of morphologies that we see in mammals. This is a very promising approach that ultimately should provide us with explanations of how genetic and epigenetic influences ultimately result in alternate shapes and structures. While many laboratories are pursuing craniofacial development to understand and ultimately reduce birth defects, such as cleft palate, few are exploring craniofacial development with a primary intent of deciphering the mechanisms behind the evolution of craniofacial form. Here, Heuze and colleagues take a mixed approach where studies of the syndromes resulting in craniosynostosis in human infants and variations in facial retrusion in domestic dogs can be used to explore evolutionary changes in New World monkeys, in particular changes in craniofacial characteristics such as facial retrusion. Methodology includes the important methods of geometric morphometrics, which are transforming our ability to explore and understand the geometry of shape change in organisms. While this study does not begin to address molecular and genetic mechanisms of shape change in the midface, it does provide important evidence that the zygomatic region of the midface can vary independently and thus has evolved somewhat independently from other portions of the midface. This is important information for then beginning to explore the genetic basis of zygomatic form. Developmental patterns can also be used to addresses issues related to phylogeny. In primate evolution, one important issue has been to determine the phylogenetic relationships of tarsiers, as these creatures appear to occupy an important position when attempting to understand the evolutionary relationships of stepsirrhine and anthropoid primates. The postorbital region of their craniofacial anatomy, which is largely adjacent to portions of the zygoma, forms a partial postorbital septum in tarsiers that unites them more closely with anthropoids than strepsirrhines, in particular large-eyed Eocene forms represented by fossils. To approach this question, Deleon et al. (2016, this issue) study and compare the perinatal postorbital anatomy of 21 genera of primates. This study was enabled by another modern technology: microct scanning, which allows inspection of threedimensional form both from external and internal aspects. The findings based on the early development and growth of the postorbital area show complex relationships among and between anthropoids, strepsirrhines, and tarsiers based on the presence and absence of the frontal spur in these groups, and the development of the posterior lamina of the zygomatic bone in anthropoids. While the work does not provide an answer to the phylogenetic question, it does provide hypotheses about developmental and growth patterns of portions of the various bones in the postorbital region that may or may not relate to functional differences, and will allow a basis for understanding variations in fossil forms that may illuminate the evolution of these major primate clades.

WHAT IS NEW ABOUT THE ZYGOMA? 1613 A largely unexplored topic in the development and growth of skeletal structures has been the influence and adaptation of patterns of vascularization. It could be that these patterns, as partially exemplified by pore structures in cortical bone, reflect patterns of bone growth and/or remodeling induced by features such as bone strain during function. Some aspects of these patterns, particularly those on periosteal surfaces, most likely reflect patterns of bone apposition during growth but may also relate to muscular and ligamentous attachments. The paper by Herring and Ochareon (2016, this issue) provides descriptions of the periosteum and associated vasculature of the zygomatic arch during growth in young pigs. The methods employed here use histological techniques to study both decalcified and undecalcified sections taken from whole mounts of zygomatic arches, some of which had been perfused with vascular fill and some of which were from animals treated with the vital bone label calcein. Outstanding images result from these techniques that allow description of some aspects of the vascularization of the arches, especially the periosteal surfaces. This area of research has been undergoing the development of new techniques in recent years in which vascular fill is infused into undecalcified bones that can then be scanned with microct, allowing a reconstruction of three-dimensional vascular patterns. This new approach, along with the classic techniques used in this article, will permit even better understanding of the structure and development of vascular patterns. The results of the study show variations in vascular patterns regionally in the zygomatic arch, such as differences between the lateral and medial sides. The authors suggest that these differences may be related to differences in related soft tissues as well as difference in development patterns or regional functions. This area of study is too new to allow for much comparative analysis, which is in part a consequence of the difficulty of the involved techniques. Perhaps advances in the three dimensional approaches mentioned above will allow future research to enable a better understanding of vascular patterns in bone. A classic technique for investigating the impact of functional variation on differences in skeletal growth in the craniofacial region has been through the use of hard and soft diet regimens. Most studies in this area have focused on the mandible or on the cranium as a whole. Here Franks et al. (2016, this issue) look at the influence of altered diet on the growth of the zygomatic arch in rabbits and pigs. The postweaning rabbit experiments had an adequate time frame and sufficient sample sizes to detect differences. The results, contrary to mandibular studies, did not show differences in cortical thicknesses in various region of the zygomatic arch between groups during growth. However, some differences were found in bone density as determined with micro-ct scans. Bone density was greater in the zygomatic arches in rabbits fed the most mechanically challenging diets. This result may be counterintuitive in that bone regions with greater and higher volumes of loading might be expected to be less dense because of increased bone remodeling resulting from the increased function. It would be interesting to see if there is internal bone remodeling in the zygomatic arches of rabbits during growth. Unfortunately, these is little research in this area for comparison and the authors are only able to contrast their results to a few studies in mice in which changes in bone strength but not morphology suggested internal adaptations in the structure of the bone matrix. What these changes may be is unknown. The pig study here had a small sample size and an insufficient time period of investigation so it is described as a pilot investigation only. Regarding variation in structure in the zygomatic arches during evolution, the authors suggest that their results imply that growth plasticity accounts for few differences in zygomatic structure among organisms. Rather differences are more likely the result of natural selection and genetic change. STRUCTURE AND BIOMECHANICS OF THE ZYGOMA AND THE ZYGOMATIC ARCH The papers in this volume regarding the structure and biomechanics of the zygoma and the zygomatic arch are primarily about primates, with the greatest emphasis on humans and their closest relatives. We will first review those papers about structure and then those about function. There is great overlap between these areas as accurate details about form and structure are needed to use modern techniques, such as finite element analysis, to test functional hypotheses. In the previous section, we reviewed the paper by Deleon et al. (2016, this volume) in which the perinatal anatomy of a large group of primates was used to understand the development of the postorbital region and it phylogenetic implications. Two further papers are also about the orbit, but with a greater emphasis on structure and function. Harvey et al. (2016, this volume) use techniques of microdissection and light microscopy to study the orbital structure of four species of strepsirrhine primates and three species of fruit bats. The goal here is to understand how large eyes in orbits without postorbital boney structures are supported by soft tissues. Further they explore the implications of this anatomy for the presence of a binocular visual field, which is important as binocular vision is not reliant on postorbital boney support in some groups of mammals. The results show that fruit bats have fascial membranes that provide ocular support sufficient to produce convergent vision, which suggests that the lack of postorbital boney structures in early primates is insufficient evidence for concluding the lack of a binocular visual field. They further suggest the importance of considering further studies of soft and hard tissues and especially the use of three-dimensional techniques for determining the relationship between orbital structure and ocular orientation. This goal is met in the second article on this topic by Rosenberger et al. (2016, this volume). They validate, through the use of studies of dry skulls and dissection of seven species of modern primates, a new method to reconstruct eye volume, placement, and orientation using three-dimensional assessments of the shape of the intra-orbital surface. This method does not require the presence of a postorbital bar. They then apply this technique to a series of fossil primates. These articles are important as they provide a structural basis for a more comprehensive analysis of vision in primate evolution. Soft tissues of the face and especially those overlying the zygomatic region are not well studied in primates. Yet they may be of great significance for understanding the evolution of facial mobility and expression in

1614 DECHOW AND WANG humans, which is one of our primary modes of communication. Burrows et al. (2016, this volume) studied histologically full thickness samples of facial soft tissues from six primate species including humans, chimpanzees, gibbons, rhesus macaques, tarsiers, and galagos. They found a distinct anatomical difference between the anthropoids and the prosimians. In the anthropoids, a connective tissue layer, which they refer to as the superficial musculo-aponeurotic system, encased the facial muscles between the skin and the deep fascia; this layer was not found in prosimians. They suggest that presence of this structure in anthropoids may be related to increased facial mobility and facial displays. A common comparative method in the study of bone biomechanics and function is to study variations in boney cross-sections including cortical area and measures of section moduli. This technique has been very informative in understanding the shape of a variety of postcranial bones and the mandible. The study by Edmonds (2016, this volume) takes this approach for exploring variations in zygomatic arch morphology in 77 individuals from 11 primate species. This approach has previously not been attempted for the zygomatic arch because collection of the data required the use of micro-ct scanning. Also essential for this work was adequate knowledge of the diet of some of these species to allow classification of closely related species as those that ate mechanically resistant versus nonmechanically resistant foods. Differences in relative cortical area as well as section moduli could then be tested between closely related species using pairwise comparisons. Differences between regions (anterior versus posterior) of the zygomatic arch were also tested within species. Overall, expected differences were found with species eating mechanically resistant foods mostly showing increased relative cortical areas and some increased section moduli. In most species, the anterior part of the zygomatic arch showed the larger relative cortical area and section moduli. This corresponds with in vivo functional tests showing greater loading on the anterior aspect of the zygomatic arch. Work such as that by Edmonds (2016, this volume) relies on concepts of beam theory in its various assumptions. While this is useful for testing hypotheses about the zygomatic arch, which can be approximated as a beamlike structure, functional hypotheses related to more complex structures such as the body of the zygoma and its frontal and maxillary processes require other approaches. The technique now coming under wide application is the use of finite element modeling, which does not make assumptions about the shape of the structure being tested. Rather this technique allows biomechanical assessment of localized strains and stresses in bone as long the structures can be modeled with accurate consideration of the loading conditions, the details of the structure and the geometry of the bone, and the elastic properties of the bone tissues. Even with this information, finite element models should be validated by comparisons with in vivo and ex vivo experiments which allow the measurements of strain to be sampled and compared between the model and the real structure on which it is based. Several papers in this volume describe the collection of data needed for finite element modeling and two others describe some of the results of finite element modeling experiments. One of these papers also reviews our knowledge of in vivo strain gage experiments related to the zygoma in primates. Elastic properties of cortical bone of the zygoma are available for humans, baboons, and rhesus monkeys. The paper by Gharpure et al. (2016, this volume) extends this comparative sample to chimpanzees. This article examines elastic properties along with bone density and cortical thickness throughout the cranium in a sample that includes four common chimpanzees and one bonobo. Differences in elastic properties, as in humans, baboons, and rhesus monkeys, are found by anatomical region. Relative regional differences vary between species, which are examined here by a detailed comparison of humans and chimpanzees. Some of the data from this study are used in the studies by Prado et al. (2016, this volume) and Smith and Grosse (2016, this volume) in the construction of their finite element models. The zygoma in primates, including humans, consists of multiple bone tissue types; namely, a trabecular core surrounded by a cortical shell. Variations in this structure have not been explored to date but are now possible through the use of micro-ct scanning. Finite element models of the zygoma have used cortical elastic properties, some of which are described by Gharpure et al. (2016, this volume), but accurate measurements of the elastic properties of the internal trabecular bone have not yet been attempted. The paper by Pryor et al. (2016, this volume) begins to address this problem. Their study compares trabecular structure in the zygoma as assessed through micro-ct scans between samples of human and chimpanzee crania. Some differences are found between these taxa, but also a wide range of variation is documented, especiallyinthechimpanzeesample,whereonecommonchimpanzee showed virtually no trabecular internal structure. Some similarities between trabecular orientations and patterns of strain determined in finite element models were noted. While this study does not measure the elastic properties of the trabecular bone in the zygoma, it is the first to assess variations in zygomatic trabecular morphology. Developmental anomalies in the zygoma provide an opportunity for interesting natural experiments regarding zygomatic function. The paper by Wang and Dechow (2016, this volume) documents a rare structural variant in zygomatic morphology; namely, the presence of an intrazygomatic suture. The incidence of this feature as well as its structure is documented in a small number of skulls taken from a large sample of rhesus monkeys, orangutans, and humans. Museum numbers are provided to facilitate further study of these unusual specimens. Though this phenomenon has been known for over centuries, craniofacial differences in these specimens are identified for the first time and the possible biomechanical consequences of this morphology are discussed providing hypotheses which can be tested using future finite element modeling experiments. The remaining two papers in this volume use finite element analysis and a review of strain gage studies to address the biomechanics of the zygoma. The paper by Smith and Grosse (2016, this volume) uses finite element models of the crania of common chimpanzees to assess the significance of variations in the shape of the zygomatic arch. The models are artificially manipulated to produce zygomatic arches that are cylindrical, elliptical, and blade-like. The patterns of strain are then examined throughout the craniofacial skeleton. The

WHAT IS NEW ABOUT THE ZYGOMA? 1615 results indicate that differences in zygomatic arch shape have large effects on strain in the arch itself but little to no effect elsewhere in the craniofacial skeleton. Thus it appears that the shape of the arch may be well adapted primarily for local functional constraints. The craniofacial skeleton has been described in a series of seminal works dating back to the beginning of the 20 th century as consisting of a framework consisting of vertical pillars and transverse buttresses. One of these pillars has been described anatomically as the boney structures that transmit compressive forces during molar biting and that consist of the zygomaticoalveolar crest on the maxilla, the zygoma, and the lateral wall of the orbit. Prado et al. (2016, this volume) review the existing structural, material property, and strain gage data and provide some new data to show that this model is a gross misconception of how the zygoma works biomechanically. The zygoma in reality has a complex mechanical function with primarily patterns of bending and shear, rather than axial compression as suggested by the pillar model. It is best not to represent the zygoma as a simple structure, such as a beam or a pillar, but rather to evaluate its complex function locally using finite element techniques. A similar analysis could likely be applied to other areas of the craniofacial skeleton and finite element models are likely to serve as optimal representations of stress and strain patterns in these regions as well. ACKNOWLEDGMENTS We thank all the authors of the papers in these two volumes on the zygoma for their hard work in producing these manuscripts and for their patience during the review process. Likewise, we thank those responsible for the careful reviews and sometimes re-reviews as we worked to put our best efforts forward. We are truly blessed with an academic community made up of outstanding individuals. We are grateful to Dr. Xing Xu, Dr. Corwin Sullivan, Mr. Yi Liu, and Mr. Lida Xing of the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences for preparing cover images. We also thank Dr. Jeffrey Laitman, the Associate Editor of The Anatomical Record who was responsible for encouraging and enabling us to produce these volumes and who with great humour and understanding kept us on task and on time. LITERATURE CITED Burrows A, Rogers-Vizene C, Li L. 2016. The mobility of the human face: more than just the musculature. Anat Rec 299:1779 1788. DeLeon V, Smith T, Rosenberger A. 2016. Ontogeny of the postorbital region in tarsiers and other primates. Anat Rec 299:1631 1645. Edmonds H. 2016. Zygomatic arch cortical area and diet in haplorhines. Anat Rec 299:1789 1800. Ellis E, 3rd, el-attar A, Moos KF. 1985. An analysis of 2.067 cases of zygomatico-orbital fracture. J Oral Maxillofac Surg 43:417 428. Elzanowski A. 2002. 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