Annie M. Burrows

On the origin, homologies and evolution of primate facial muscles, with a particular focus on hominoids and a suggested unifying nomenclature for the facial muscles of the Mammalia

The mammalian facial muscles are a subgroup of hyoid muscles (i.e. muscles innervated by cranial nerve VII). They are usually attached to freely movable skin and are responsible for facial expressions. In this study we provide an account of the origin, homologies and evolution of the primate facial muscles, based on dissections of various primate and non‐primate taxa and a review of the literature. We provide data not previously reported, including photographs showing in detail the facial muscles of primates such as gibbons and orangutans. We show that the facial muscles usually present in strepsirhines are basically the same muscles that are present in non‐primate mammals such as tree‐shrews. The exceptions are that strepsirhines often have a muscle that is usually not differentiated in tree‐shrews, the depressor supercilii, and lack two muscles that are usually differentiated in these mammals, the zygomatico‐orbicularis and sphincter colli superficialis. Monkeys such as macaques usually lack two muscles that are often present in strepsirhines, the sphincter colli profundus and mandibulo‐auricularis, but have some muscles that are usually absent as distinct structures in non‐anthropoid primates, e.g. the levator labii superioris alaeque nasi, levator labii superioris, nasalis, depressor septi nasi, depressor anguli oris and depressor labii inferioris. In turn, macaques typically lack a risorius, auricularis anterior and temporoparietalis, which are found in hominoids such as humans, but have muscles that are usually not differentiated in members of some hominoid taxa, e.g. the platysma cervicale (usually not differentiated in orangutans, panins and humans) and auricularis posterior (usually not differentiated in orangutans). Based on our observations, comparisons and review of the literature, we propose a unifying, coherent nomenclature for the facial muscles of the Mammalia as a whole and provide a list of more than 300 synonyms that have been used in the literature to designate the facial muscles of primates and other mammals. A main advantage of this nomenclature is that it combines, and thus creates a bridge between, those names used by human anatomists and the names often employed in the literature dealing with non‐human primates and non‐primate mammals.

Histological definition of the vomeronasal organ in humans and chimpanzees, with a comparison to other primates

The vomeronasal organ (VNO) is a chemosensory structure that has morphological indications of functionality in strepsirhine and New World primates examined to date. In these species, it is thought to mediate certain socio‐sexual behaviors. The functionality and even existence of the VNO in Old World primates has been debated. Most modern texts state that the VNO is absent in Old World monkeys, apes, and humans. A recent study on the VNO in the chimpanzee (Smith et al., 2001b ) challenged this notion, demonstrating the need for further comparative studies of primates. In particular, there is a need to establish how the human/chimpanzee VNO differs from that of other primates and even nonhomologous mucosal ducts. Histochemical and microscopic morphological characteristics of the VNO and nasopalatine duct (NPD) were examined in 51 peri‐ and postnatal primates, including humans, chimpanzees, five species of New World monkeys, and seven strepsirhine species. The nasal septum was removed from each primate and histologically processed for coronal sectioning. Selected anteroposterior intervals of the VNO were variously stained with alcian blue (AB)‐periodic acid‐Schiff (PAS), PAS only, Gomori trichrome, or hematoxylin‐eosin procedures. All strepsirhine species had well developed VNOs, with a prominent neuroepithelium and vomeronasal cartilages that nearly surrounded the VNO. New World monkeys had variable amounts of neuroepithelia, whereas Pan troglodytes and Homo sapiens had no recognizable neuroepithelium or vomeronasal nerves (VNNs). Certain unidentified cell types of the human/chimpanzee VNO require further examination (immunohistochemical and electron microscopic). The VNOs of P. troglodytes, H. sapiens, and New World monkeys exhibited different histochemistry of mucins compared to strepsirhine species. The nasopalatine region showed great variation among species. It is a blind‐ended pit in P. troglodytes, a glandular recess in H. sapiens, a mucous‐producing duct in Otolemur crassicaudatus, and a stratified squamous passageway in all other species. This study also revealed remarkable morphological/histochemical variability in the VNO and nasopalatine regions among the primate species examined. The VNOs of humans and chimpanzees had some structural similarities to nonhomologous ciliated gland ducts seen in other primates. However, certain distinctions from the VNOs of other primates or nonhomologous epithelial structures characterize the human/chimpanzee VNO: 1) bilateral epithelial tubes; 2) a superiorly displaced position in the same plane as the paraseptal cartilages; 3) a homogeneous, pseudostratified columnar morphology with ciliated regions; and 4) mucous‐producing structures in the epithelium itself. Anat Rec 267:166–176, 2002.

A rabbit model of human familial, nonsyndromic unicoronal suture synostosis. II. Intracranial contents, intracranial volume, and intracranial pressure

This two-part study reviews data from a recently developed colony of New Zealand white rabbits with familial, nonsyndromic unilateral coronal suture synostosis, and this second part presents neuropathological findings and age-related changes in intracranial volume (ICV) and intracranial pressure (ICP) in 106 normal rabbits and 56 craniosynostotic rabbits from this colony. Brain morphology and anteroposterior length were described in 44 rabbit fetuses and perinates (27 normal; 17 synostosed). Middle meningeal artery patterns were qualitatively assessed from 2-D PCC MRI VENC scans and endocranial tracings from 15, 126-day-old rabbits (8 normal, 7 rabbits with unicoronal synostosis). Brain metabolism was evaluated by assessing 18F-FDG uptake with high-resolution PET scanning in 7, 25-day-old rabbits (3 normal, 4 with unicoronal or bicoronal synostosis). Intracranial contents and ICV were assessed using 3-D CT scanning of the skulls of 30 rabbits (20 normal,10 with unicoronal synostosis) at 42 and 126 days of age. Serial ICP data were collected from 66 rabbits (49 normal; 17 with unicoronal synostosis) at 25 and 42 days of age. ICP was assessed in the epidural space using a Codman NeuroMonitor microsensor transducer. Results revealed that cerebral cortex morphology was similar between normal and synostosed fetuses around the time of synostosis. Significantly (P<0.05) decreased A-P cerebral hemisphere growth rates and asymmetrical cortical remodeling were noted with increasing age in synostotic rabbits. In addition, rabbits with unicoronal suture synostosis exhibited asymmetrical middle meningeal artery patterns, decreased and asymmetrical brain metabolism, a “beaten-copper” intracranial appearance, significantly (P<0.05) decreased ICV, and significantly (P<0.01) elevated ICP compared with normal control rabbits. The advantages and disadvantages of these rabbits as a model for human familial, nonsyndromic unicoronal suture synostosis are discussed, especially in light of recent clinical neuropathological, ICV, and ICP findings recorded in human craniosynostotic studies.

Prenatal Growth of the Human Vomeronasal Organ

Vomeronasal organs (VNOs) are paired epithelial structures located adjacent to the nasal septum that form in the late first trimester of human fetal development. Although VNOs have long been known to exist in fetal and adult humans, some studies continue to suggest that these structures may be degenerative or functionless. Little is known of the growth of the VNO.

A rabbit model of human familial, nonsyndromic unicoronal suture synostosis. I. Synostotic onset, pathology, and sutural growth patterns

Poswillo has stated, “The more severe anomalies of the calvaria, such as plagiocephaly, Crouzon [syndrome], and Apert syndrome still defy explanation, in the absence of an appropriate animal system to study” (p. 207). This two-part study reviews data from a recently developed colony of New Zealand white rabbits with familial, nonsyndromic unilateral coronal suture synostosis. Part 1 presents pathological findings and compensatory sutural growth data from 109 normal rabbits and 82 craniosynostotic rabbits from this colony. Synostotic foci, onset, and progression were described in the calvariae from 102 staged (fetal days 21, 25, 27, 33; term = 30 days) fetuses (39 normal, 63 synostosed). Calvarial suture growth patterns from 10 to 126 days of age were assessed from serial radiographs obtained from 89 rabbits (70 normal rabbits and 19 rabbits with unicoronal suture synostosis) with amalgam bone marker implants. Perinatal results revealed that by fetal day 25 the synostotic focal point in synostotic rabbits consistently originated from the endocortical surface of the calvaria in the middle of the coronal suture at a presumed high-tension, interdigitating zone. Histological analysis revealed hyperostotic osteogenic fronts on the affected side compared with the unaffected side. Postnatal sutural growth data revealed a predictable pattern of plagiocephaly (contralateral coronal sutures growing more than ipsilateral sutures and ipsilateral frontonasal and anterior lambdoidal sutures growing more than contralateral sutures), which resulted in early cranial vault deformities and a double “S” shape torquing towards the affected side. The advantages and disadvantages of these rabbits as a model for human familial, nonsyndromic unicoronal suture synostosis are discussed, especially in light of recent cytokine and genetic findings from human craniosynostotic studies.

Searching for the vomeronasal organ of adult humans: preliminary findings on location, structure, and size.

The adult human vomeronasal organ (VNO) has been the focus of numerous recent investigations, yet its developmental continuity from the human fetal VNO is poorly understood. The present study compared new data on the adult human “VNO” with previous findings on the fetal human VNO. Nasal septa were removed from twelve adult human cadavers and each specimen was histologically sectioned. Coronal sections were stained with hematoxylin‐eosin and periodic acid‐Schiff‐hematoxylin. The sections were examined by light microscopy for the presence of VNOs and the anterior paraseptal cartilages (PC). VNOs were quantified using a computer reconstruction technique to obtain VNO length, volume, and vomeronasal epithelium (VNE) volume. Histologically, VNOs and PCs were identified in eleven specimens. VNOs had ciliated, pseudostratified columnar epithelium with goblet cells. Variations (e.g., multiple communications to the nasal cavity) were observed in several specimens. Quantification was possible for 16 right or left VNOs. Right or left VNOs ranged from 3.5 to 11.8 mm in length, from 1.8 to 33.8 x 10‐4cc in volume, and from 2.7 to 18.1 x 10‐4cc in VNE volume. Results indicated that the adult human VNO was similar in VNE morphology, lumen shape, and spatial relationships when compared to human fetal VNOs. By comparison with previous fetal VNO measures, mean VNO length, volume, and VNE volume were larger in adult humans. These results support previous suggestions that postnatal VNO growth occurs. Findings on location and spatial relationships of the adult VNO were similar to those seen in human fetuses, but critical questions remain regarding the ontogeny of the vomeronasal nerves and VNE. Microsc. Res. Tech. 41:483–491, 1998.

The existence of the vomeronasal organ in postnatal chimpanzees and evidence for its homology with that of humans

It is currently thought that New World monkeys, prosimians, and humans are the only primates to possess vomeronasal organs (VNOs) as adults. Recent studies of the human VNO suggest that previous investigations on Old World primates may have missed the VNO. We examined nasal septa from the chimpanzee (Pan troglodytes) grossly and histologically for comparison with nasal septa from humans, Old World monkeys (Macaca fascicularis, M. nemistrina) and prosimian primates (Microcebus murinus, Otolemur garnettii). Grossly, chimpanzees had depressions on the nasal septum similar to fossae reported anterior to the VNO openings in humans. Histologically, chimpanzees and humans had bilateral epithelial tubes which were above the superior margin of the paraseptal cartilages (vomeronasal cartilage homologue). The epithelial tubes had a homogeneous ciliated epithelium. These structures were thus positionally and structurally identical to the human VNO and unlike the well‐developed prosimian VNOs which were surrounded by vomeronasal cartilage. Macaques had no structures which resembled the VNO of either the prosimians or humans. The results demonstrate that the VNO is present postnatally in the chimpanzee and is almost identical to the human VNO in its anatomical position and histological structure. This in turn suggests that the reported absence of the VNO in at least some adult Old World primates is artifactual, and that further study may provide evidence for its existence in other species.

Anatomical position of the vomeronasal organ in postnatal humans.

In the last decade or so, there has been a renewed interest in the adult human vomeronasal organ (VNO). Studies have yielded sometimes disparate findings about the microscopic structure of the organ and its supporting tissues. Such varied descriptions may be due to examination of different regions of the VNO, individual variation of VNOs among humans, or the presence of multiple, non-homologous structures that bear false resemblance to the human VNO. A histological description of the spatial relationship of the human VNO to other nasal septal elements is needed to ensure that all investigators are examining the same regions and homologous structures. Histologically sectioned nasal septa from, 22 human cadavers (1 child, 21 adults) were examined grossly and by light microscopy for the VNO. Using histological sections, the position of the VNO relative to other structures was estimated. Sections containing the VNO were retrospectively compared to scaled photographic slides of the unsectioned septa to identify surface landmarks. Human VNOs varied in anteroposterior and superoinferior position relative to the anterior nasal spine and the nasal cavity floor. In the absence of a visible duct opening, the only reliable surface marker, no consistent surface markings were noted for precise location. VNOs were frequently found superior to swellings associated with the paraseptal and/or septal cartilages. Such findings demonstrate that the human VNO is positionally variable, which may have contributed to previous conflicting findings on presence versus absence. Furthermore, our findings support recent suggestions that the VNO may have been misidentified by some investigators, and that its opening can be easily confused with other structures.

Sutural bone frequency in synostotic rabbit crania.

This study tests the hypothesis that crania with synostosed sutures will have a significantly higher incidence of calvarial sutural bones than normal crania. Sutural bones were counted in seven calvarial sutures and compared among four groups of adult New Zealand white rabbit skulls: normal in-colony (NI) controls (N = 14), normal out-colony (NO) controls (N = 12), skulls with familial delayed onset (DO) coronal synostosis (N = 25), and skulls with experimentally immobilized coronal sutures (EI) (N = 20). Comparisons among groups were made with a Kruskal-Wallis one-way ANOVA and between groups with a Mann-Whitney U-test, using a Bonferroni correction for multiple comparisons. Significant differences (P < 0.05) were noted only in the coronal and sagittal sutures, with EI crania having the greatest number of coronal sutural bones; between group differences were undetectable for sagittal sutural bones. A post hoc two-sample binomial test for equal proportions showed that the distribution of coronal sutural bones among individuals across groups was even, while the distribution of sagittal sutural bones was significantly higher in EI crania. These results suggest that altered sutural forces of the calvaria contribute to an increased occurrence of sutural bones. However, the influence of inheritance on increased occurrence of sutural bones cannot be discounted, as reflected in the equivalent number of individuals across groups that possessed coronal sutural bones.

Prenatal Growth and Adult Size of the Vomeronasal Organ in Mouse Lemurs and Humans

Previous studies of VNO size have primarily sought to compare the magnitude of VNO function (via a presumed link between VNO size and receptor population) among vertebrate species (Dawley, 1998) and sexes (Dawley and Crowder, 1995; Weiler et al., 1999). A few have sought to determine whether the structure degenerates or persists in humans. These studies have described a continuous increase in prenatal VNO anteroposterior length and epithelial volume (Smith et al., 1996, 1997; Sherwood et al., 1999), especially during the late second and third trimesters (Smith et al., 1997). A comparison of prenatal VNO data with the same measures in adults indicates that some postnatal growth, of variable magnitude, occurs during postnatal human ontogeny (Smith et al., 1998; Bhatnagar and Smith, in preparation). Although these studies have established that the human VNO does not degenerate (prenatally or postnatally), no studies have attempted to determine the magnitude of human VNO growth via a comparison to other species.