Primate Skull Research Articles

An all-ultrasound cranial imaging method to establish the relationship between cranial FUS incidence angle and transcranial attenuation in non-human primates in 3D

Focused ultrasound (FUS) is a non-invasive and non-ionizing technique which deploys ultrasound waves to induce bio-effects. When paired with acoustically active particles such as microbubbles (MBs), it can open the blood brain barrier (BBB) to facilitate drug delivery otherwise inhibited due to the presence of BBB. One of the parameters that affects the FUS beam propagation is the beam incidence angle on the skull. Prior work by our group has shown that, as incidence angles deviate from 90°, FUS focal pressures attenuate and result in a smaller BBB opening volume. The incidence angles calculated in our prior studies were in 2D and used skull information from CT. The study presented herein develops methods to calculate incidence angle in 3D in non-human primate (NHP) skull fragments using harmonic ultrasound imaging without using ionizing radiation. Our results show that ultrasound harmonic imaging is capable of accurately depicting features such as sutures and eye-sockets of the skull. Furthermore, we were able to reproduce previously reported relationships between the incidence angle and FUS beam attenuation. We also show feasibility of performing ultrasound harmonic imaging in in-vivo non-human primates. The all-ultrasound method presented herein combined with our neuronavigation system stands to increase more widespread adoption of FUS and render it accessible by eliminating the need for CT cranial mapping.

Tourism, international wildlife trade and the (in)effectiveness of CITES

SummaryThere are clear links between tourism and the international wildlife trade, especially in countries with high levels of biodiversity and high numbers of international tourists. In the absence of clear regulations and implementation of existing policies, tourists can inadvertently have a negative impact on the environment, including through items bought as souvenirs. Bali is one of the world’s premier tourist destinations. We investigated legally protected species that are offered for sale specifically targeting tourists in Bali. During December 2022–June 2023, we surveyed 66 shops offering curios (skulls, bones, carvings) of animals for which the international trade is regulated by the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES). We found items from >500 individuals of 20 CITES-listed species, including primate skulls, ivory carvings and decorated shells. According to vendors, there would be no problem exporting these items despite the absence of CITES permits. Export records over the last two decades provided by the Indonesian authorities, mostly indicating no exports, contrast sharply with our observations in Bali. A short but effective campaign as a collaborative effort between industry, tourism operators, local and expatriate communities and government agencies could result in a drastic reduction of protected and/or CITES-listed species ending up in trade.

Follow Your Nose: Ontogeny of the Olfactory Duct in Primates

Most primates are characterized by orbital convergence, the displacement of the orbits toward the rostral midline. In platyrrhine primates and tarsiers, this convergence is so extreme that orbits meet in the midline at the apical interorbital septum. This produces a spatial separation of the anterior cranial fossa and the nasal cavity. The olfactory bulbs of the brain pass dorsal and then rostral to the orbits to reach the nasal cavity via a bony tube, the olfactory duct. Nerves are expected to constrain growth of musculoskeletal structures. We hypothesized that the network of olfactory nerves effectively tethers the olfactory bulbs to the mucosa of the nasal cavity, and the growth of facial structures in these primates results in rostral displacement of the olfactory bulbs through ontogeny. In addition, growth of the midface may be constrained by this functional relationship.This comparative analysis was based on 3D reconstructions of cranial structures in newborns and adults from representative platyrrhine species (e.g., Aotus nancymaae and Cebuella pygmaea) and tarsiers (Tarsius syrichta). Spatial relationships of the olfactory duct were estimated using endocasts based on conventional microCT scans. In addition, diffusion iodine contrast‐enhanced CT (diceCT) images were used to study Aotus nancymaae at multiple stages of ontogeny. DiceCT allowed us to reconstruct the actual position of olfactory bulbs relative to the olfactory duct and the distribution of olfactory nerves in the nasal cavity. 3DSlicer and Blender software were used to render 3D models. These data confirm our hypothesis that the rostral projection of the olfactory bulbs relative to the frontal lobes of the brain increases through ontogeny. In addition, the paths of olfactory nerves are diverted around the convergent eyes. The ontogenetic relationships occurring in platyrrhine and tarsier olfactory ducts have evolutionary implications for biological variation in the primate skull.

Optimizing Newborn Primate Endocast Reconstruction in 3DSlicer

Natural and artificial endocasts have been used for decades to enable researchers to visualize the endocranial space and approximate the morphology of internal soft tissue structures. Producing an endocast of the newborn primate skull is made difficult by the large fontanelle spaces between growing bones. As there is no definitive endocranial boundary, these spaces have the potential to introduce error into both manual and semi‐automatic methods of endocast reconstruction.This study examines three methods of capturing endocranial volume (EV) from the endocasts of multiple species of newborn primates. For each specimen an EV was produced using three methods: a) manual, b) semi‐automatic and c) “patched” semi‐automatic segmentation. Manual segmentation is considered the “gold standard” of endocast reconstruction, however it lacks the efficiency of semi‐automatic methods. The “patched” method proposed here is a novel approach to fontanelle closure that is accomplished using the “Baffle Planner” module in 3DSlicer, an open‐access post‐processing software that is freely accessible to all researchers. The interosseous patches constructed from user‐defined landmarks are placed around the ossifying edges of the fontanelle and reflect the curvature of adjacent bones.In this study we provide guidance for optimizing the parameters of newborn primate endocast reconstruction in open‐access software. Our study found both quantitative and qualitative differences between the models produced by these methods suggesting the chosen method of reconstruction affects the resulting EV measurement. We conclude that a patched semi‐automatic approach with minimal baffles appears to reflect the anatomy with sufficient accuracy, while increasing efficiency and repeatability.

Transcranial Theranostic Ultrasound for Pre-Planning and Blood-Brain Barrier Opening: A Feasibility Study Using an Imaging Phased Array In Vitro and In Vivo.

This study aims to demonstrate a pre-planning pipeline consisting of transcranial simulations and in vitro experimentation used to inform synchronous BBB opening and power cavitation imaging (PCI) with a single theranostic ultrasound (TUS) phased array. Acoustic wave propagation simulation findings of pressure attenuation and focal shift through clinical-CT and micro-CT-based primate skull models were compared, while the latter were used to determine the impact of beam steering angle on focal shift and pressure attenuation. In vitro experimentation with a channel phantom enabled characterization of skull-induced receive focal shift (RFS), while in vivo BBB opening and PCI using in silico and in vitro pre-planning information was conducted using a custom Verasonics/MATLAB script. Simulations confirmed steering angle dependent transcranial focal shift and pressure attenuation, while in vitro experiments revealed minimal (0.30-1.50 mm) skull-induced RFS. In vivo rodent experiments with overlaid primate skull fragments demonstrated successful TUS-mediated BBB opening and spatially correlated power cavitation images (PCI) with regions of BBB opening on T1-weighted magnetic resonance images (MRI). We demonstrated the feasibility for TUS-mediated BBB opening in vivo using in silico and in vitro pre-planning information. TUS as an ultrasound-guided modality for BBB opening could serve as a promising alternative to current FUS-mediated BBB opening configurations in the clinic.

Cranial Anatomical Integration and Disparity Among Bones Discriminate Between Primates and Non-primate Mammals

The primate skull hosts a unique combination of anatomical features among mammals, such as a short face, wide orbits, and big braincase. Together with a trend to fuse bones in late development, these features define the anatomical organization of the skull of primates—which bones articulate to each other and the pattern this creates. Here, I quantified the anatomical organization of the skull of 17 primates and 15 non-primate mammals using anatomical network analysis to assess how the skulls of primates have diverged from those of other mammals, and whether their anatomical differences coevolved with brain size. Results show that primates have a greater anatomical integration of their skulls and a greater disparity among bones than other non-primate mammals. Brain size seems to contribute in part to this difference, but its true effect could not be conclusively proven. This supports the hypothesis that primates have a distinct anatomical organization of the skull, but whether this is related to their larger brains remains an open question.

Testing the damage caused by a golden eagle (Aquila chrysaetos) on a primate skull: A taphonomic case study of the bone damage observed after a simulated predatory attack

AbstractThe present case study proposes an experimental approach to the taphonomic characterization of modifications that are produced on bone surfaces by eagles during the attack and capture of their prey. Under these circumstances, a golden eagle (Aquila chrysaetos) attack on a Barbary macaque (Macaca sylvanus) skull was simulated. The macaque specimen was analysed from a taphonomic perspective, which allowed for the comparison of traces left on the skull against the data that have already been published on past and present primate attacks by eagles. The results of the experiment confirmed the presence of some modifications that were similar to the damage described in the literature for specific palaeoanthropological specimens. However, the number of alterations observed was much lower because the attack was restricted to a single event, with the aim being to isolate the specific predatory attack damage. This kind of experiment demonstrates how experimental archaeology can be a useful tool for replicating past scenarios by using rigorous scientific methods, testing hypotheses and interpreting archaeological assemblages.

Endomaker, a new algorithm for fully automatic extraction of cranial endocasts and the calculation of their volumes.

Reproducing cranial endocasts is a major goal of researchers interested in vertebrate brain evolution. We present a new R software, named endomaker, which allows the automatic extraction of endocasts from skull meshes along with the calculation of its volume. We applied endomaker on non-primate and primate skulls including the Australopithecus africanus specimen Sts-5. We proved endomaker is faster, more feature-rich and possibly more accurate than competing software. Endomaker is the only available program endowed with the possibility to process an entire mesh directory straight away, promising to expand the scope and phylogenetic breadth of comparative studies of brain evolution.

Effects of different segmentation methods on geometric morphometric data collection from primate skulls

Abstract An increasing number of studies are analysing the shapes of objects using geometric morphometrics with tomographic data, which are often segmented and transformed to three‐dimensional (3D) surface models before measurement. This study aimed to evaluate the effects of different image segmentation methods on geometric morphometric data collection using computed tomography data collected from non‐human primate skulls. Three segmentation methods based on a visually selected threshold, a half‐maximum height protocol and a gradient and watershed algorithm were compared. For each method, the efficiency of surface reconstruction, the accuracy of landmark placement and the level of variation in shape and size compared with various levels of biological variation were evaluated. The visual‐based method inflated the surface in high‐density anatomical regions, whereas the half‐maximum height protocol resulted in a large number of artificial holes and erosion. However, the gradient‐based method mitigated these issues and generated the most efficient surface model. The segmentation method used had a much smaller effect on shape and size variation than interspecific and inter‐individual differences. However, this effect was statistically significant and not negligible when compared with intra‐individual (fluctuating asymmetric) variation. Although the gradient‐based method is not widely used in geometric morphometric analyses, it may be one of promising options for reconstructing 3D surfaces. When evaluating small variations, such as fluctuating asymmetry, care should be taken around combining 3D data that were obtained using different segmentation methods.

Phenotypic plasticity in the mandibular morphology of Japanese macaques: captive-wild comparison.

Despite the accumulating evidence suggesting the importance of phenotypic plasticity in diversification and adaptation, little is known about plastic variation in primate skulls. The present study evaluated the plastic variation of the mandible in Japanese macaques by comparing wild and captive specimens. The results showed that captive individuals are square-jawed with relatively longer tooth rows than wild individuals. We also found that this shape change resembles the sexual dimorphism, indicating that the mandibles of captive individuals are to some extent masculinized. By contrast, the mandible morphology was not clearly explained by ecogeographical factors. These findings suggest the possibility that perturbations in the social environment in captivity and resulting changes of androgenic hormones may have influenced the development of mandible shape. As the high plasticity of social properties is well known in wild primates, social environment may cause the inter- and intra-population diversity of skull morphology, even in the wild. The captive–wild morphological difference detected in this study, however, can also be possibly formed by other untested sources of variation (e.g. inter-population genetic variation), and therefore this hypothesis should be validated further.

Description and Analysis of Spatial Patterns in Geometric Morphometric Data

The development of techniques for the acquisition of high-resolution 3D images, such as computed tomography and magnetic resonance imaging, has opened new avenues to the study of complex morphologies. Detailed descriptions of internal and external traits can be now obtained, allowing the intensive sampling of surface points. In this paper, we introduce a morphometric and statistical framework, grounded on Procrustes and Procrustes-like techniques as well as standard spatial statistics, to explicitly describe and incorporate the spatial pattern of these surface points into the analyses. We exemplified this approach by analyzing ontogenetic changes in a sample of human brain endocasts and inter-specific differences between primate skulls. An intensive sampling of points on 3D surfaces was performed by automatic techniques and the morphometric variation among specimens was measured by the residuals obtained after the alignment of points. Our results showed that shape changes in both examples are spatially structured. Different results were attained by using methods that incorporate or not the spatial structure in the evaluation of the effect of specific biological factors on shape variation. Particularly, these analyses indicated that the effect of biological factors acting at local scales can be confounded with more systemic factors (by example, the effect of the diet on the facial skeleton) if the spatial structure is not taken into account. Overall, our results suggest that the intensive description of shape differences among structures using densely sampled points on 3D surfaces combined with spatial statistical methods can be used to explore problems not widely addressed in morphological studies.

All things bleak and bare beneath a brazen sky: practice and place in the analysis of Australopithecus.

The fossilized primate skull known as the Taungs Baby, discovered in South Africa, was put forward in 1925 as a controversial 'missing link' between humans and apes. This essay examines the controversy generated by the fossil, with a focus on practice and the circulation of material objects. Viewing the Taungs story from this perspective provides a new outlook on debates, one that suggests that attention to the importance of place, particularly the ways that specific localities shape scientific practices, is crucial to understanding such controversies. During the 1920s, the fossil itself did not move or circulate from its South African location, a fact that raised methodological concerns in understanding its significance and drew immense criticism from a range of experts. Examining the criticisms regarding the fossil's failure to circulate draws attention to the importance of centers of accumulation in the analysis of hominid fossils. Diverging from existing histories that primarily emphasize the role of theory in paleoanthropological debates, then, this article argues that scientific practice played an important role in the Taungs fossil controversy. Examining this dimension of the debates has broader implications for revealing the underlying imperial assumptions that guided hominid paleontology during the early twentieth century.

A New Tool for Digital Alignment in Virtual Anthropology.

The study of the fossil record is fundamental to understand the evolution of traits. Because fossil remains are often fragmented and/or deformed by taphonomic processes, a preliminary realignment of their constituent parts is often necessary to properly interpret their shapes. In virtual anthropology, these procedures are carried out using digital models of the remains. We present a new semi-automatic alignment R software, Digital Tool for Alignment (DTA), which uses the shape information contained in a reference sample to find the best alignment solution for the disarticulated regions. We tested DTA on three different case-studies: (1) a sample of 14 primate species including both male and female individuals, (2) a simulated, disarticulated skull of Homo sapiens, and (3) a real disarticulated human fossil specimen, Amud 1 (Homo neanderthalensis). In the first case study, we simulated disarticulation directly on digital models of the primate skulls and tested alignment quality as a function of phylogenetic proximity, sex, and body size. In the second, we compared DTA to manual alignments conducted for the same digital models. Finally, we performed DTA on a real-world case study. We found that phylogenetic proximity provides is the most important factor for alignment efficiency. However, sex and allometric effects might also be important and should therefore be taken into account at selecting reference models for alignments. DTA performs at least as well as manual alignments. Yet, as compared to manual procedures, it is faster, requires no prior anatomical knowledge and expertise and allows indefinite manipulation of the fossil items. Anat Rec, 302:1104-1115, 2019. © 2019 Wiley Periodicals, Inc.

Egg Model Training Protocol for Stereotaxic Neurosurgery and Microelectrode Implantation.

Neuroscience research uses neurosurgery in animal models for several experimental techniques. To our knowledge, there is no published method for small animal neurosurgery training. Based on the similar thickness of chicken eggshells and mouse, rat, and some small primate skulls, here we propose an egg model training protocol for stereotaxic surgery. To perform training it was used a boiled egg and the same materials needed to perform stereotaxic neurosurgery in small animals. This protocol allows trainees in neuroscience research to become familiar with the microsurgery setting and learn neurosurgery techniques, such as craniotomy drilling, dura mater removal, and electrode implantation. Egg model suitably mimics animal neurosurgery for the replacement and sparing of animals intended for training in neurosurgical skills.

The relationship of cranial, orbital and nasal cavity size with the morphology of the supraorbital region in modern Homo sapiens.

Morphological variation of the supraorbital region (SR) in human crania has been investigated and its potential sources suggested, along with the importance of the size of the facial skeleton, neurocranium, and orbit for the formation of this region. However, previous studies have not indicated whether facial size exhibits a stronger association with SR robusticity than neurocranial size or sex; moreover, the association between orbital volume and SR robusticity has been analysed only in non-human primate skulls. In this study we investigate whether the size of the facial skeleton, neurocranium, two measures of relative orbital size (orbital volume and estimated orbital aperture area), the relative size of the nasal cavity, and the relative estimated area of the anterior nasal cavity opening are related to SR robusticity; we also examine which of these analysed relationships is strongest, as well as independent of the influence of the other traits, in a geographically diverse modern human cranial sample. The results of Spearman's rank and partial rank correlations (encompassing models including or excluding sex and geographic origin) show a relationship between most of the above-mentioned variables and SR robusticity, with the exception of the estimated relative area of the orbital opening (in the case of the results of Spearman's rank correlations) and the traits of the nasal cavity. Of all the analysed traits, sex appears to be the most important for the formation of SR robusticity and, of two measures of cranial size, neurocranial size was the most significant. The strong relationship between SR robusticity and relative orbital volume was observed in models without the geographic origin factor. The results concerning analysed models suggest the influence of this factor on this relationship; however, to explain this influence, further studies are needed.

A Landmark-Free Method for Three-Dimensional Shape Analysis.

BackgroundThe tools and techniques used in morphometrics have always aimed to transform the physical shape of an object into a concise set of numerical data for mathematical analysis. The advent of landmark-based morphometrics opened new avenues of research, but these methods are not without drawbacks. The time investment required of trained individuals to accurately landmark a data set is significant, and the reliance on readily-identifiable physical features can hamper research efforts. This is especially true of those investigating smooth or featureless surfaces.MethodsIn this paper, we present a new method to perform this transformation for data obtained from high-resolution scanning technology. This method uses surface scans, instead of landmarks, to calculate a shape difference metric analogous to Procrustes distance and perform superimposition. This is accomplished by building upon and extending the Iterative Closest Point algorithm. We also explore some new ways this data can be used; for example, we can calculate an averaged surface directly and visualize point-wise shape information over this surface. Finally, we briefly demonstrate this method on a set of primate skulls and compare the results of the new methodology with traditional geometric morphometric analysis.

A collection of non-human primate computed tomography scans housed in MorphoSource, a repository for 3D data

A dataset of high-resolution microCT scans of primate skulls (crania and mandibles) and certain postcranial elements was collected to address questions about primate skull morphology. The sample consists of 489 scans taken from 431 specimens, representing 59 species of most Primate families. These data have transformative reuse potential as such datasets are necessary for conducting high power research into primate evolution, but require significant time and funding to collect. Similar datasets were previously only available to select research groups across the world. The physical specimens are vouchered at Harvard’s Museum of Comparative Zoology. The data collection took place at the Center for Nanoscale Systems at Harvard. The dataset is archived on MorphoSource.org. Though this is the largest high fidelity comparative dataset yet available, its provisioning on a web archive that allows unlimited researcher contributions promises a future with vastly increased digital collections available at researchers’ finger tips.

Anatomical network analysis shows decoupling of modular lability and complexity in the evolution of the primate skull.

Modularity and complexity go hand in hand in the evolution of the skull of primates. Because analyses of these two parameters often use different approaches, we do not know yet how modularity evolves within, or as a consequence of, an also-evolving complex organization. Here we use a novel network theory-based approach (Anatomical Network Analysis) to assess how the organization of skull bones constrains the co-evolution of modularity and complexity among primates. We used the pattern of bone contacts modeled as networks to identify connectivity modules and quantify morphological complexity. We analyzed whether modularity and complexity evolved coordinately in the skull of primates. Specifically, we tested Herbert Simon’s general theory of near-decomposability, which states that modularity promotes the evolution of complexity. We found that the skulls of extant primates divide into one conserved cranial module and up to three labile facial modules, whose composition varies among primates. Despite changes in modularity, statistical analyses reject a positive feedback between modularity and complexity. Our results suggest a decoupling of complexity and modularity that translates to varying levels of constraint on the morphological evolvability of the primate skull. This study has methodological and conceptual implications for grasping the constraints that underlie the developmental and functional integration of the skull of humans and other primates.

Anatomical Network Analysis of Primate Skull Morphology

A core question driving studies of primate evolution is how phenotypic variation in the skull arose without compromising vital functions and structures of the head. Alongside morphogenetic processes, mechanical forces influence head development, e.g. bone connections are primary growth sites and force-diffusors. Yet the influence that physical constraints (i.e., bone-bone contacts) have on the developmental plasticity and thus evolvability of skull form is unclear. Anatomical Network Analysis (AnNA) is a new way to query this influence by measuring presence, strength, direction, symmetry and density of connections among skull bones. Here we present AnNA of interaction among skull bones in twenty extant primate taxa, including humans, chosen to represent the phenotypic breadth of head variation. AnNA found that connectivity was more variable for the facial bones, which divided into three modules (midfacial, palatal, rostral) in non-human primates (a single module in humans); and more conserved for the cranial bones, which formed a single module in all primates but varied in specific bone-bone connections in Hominidae. Network models of the skull did not carry significant phylogenetic signals, stressing the influence of other factors in the evolution of skull anatomy. Our AnNA results also suggested that modularity and complexity do not evolve in a positive feedback relationship in the primate skull. Natural Sciences & Engineering Research Council of Canada (JCB); Howard University (RD); Cavanilles Institute of Biodiversity & Evolutionary Biology (BE-A, DR-G)

Lessons from the Past: Metabolic Bone Disease in Historical Captive Primates

Primate welfare in captivity has significantly improved over the last century as a result of the advances made in providing an adequate diet and environment. The skeletal collections of museums provide evidence of this shift in captive care, because metabolic disease caused by dietary deficiency or inappropriate surroundings can cause deformation to the hard tissues. The Royal College of Surgeons of England (RCS) holds a collection of 1507 nonhuman primate skulls in its Odontological Collection, the majority donated before the mid-20th century from various sources. We observed a recurring gross pathology in 51 of these skulls, noted in museum records as captive animals. In all cases, general bone thickening with decreased bone density is the main feature and involves primarily the bones of the maxillofacial region and mandible. We performed computed tomography scanning on a subsample of these skulls to investigate these pathological features further. We compared the RCS historical collections and a more recent captive primate collection at the National Museum of Scotland. The findings suggest that a metabolic bone disease is the causative agent, with osteomalacia the likely diagnosis. Osteomalacia typically occurs due to malnutrition and/or insufficient ultraviolet light exposure and in this case reflects the inadequacy of zoo primate management during the late 19th and early 20th centuries. Developments have since been made in captive animal welfare as a result of improvements in nutrition and environment. Metabolic bone disease in primate captivity can be regarded as a lesson from the past.