Trabecular bone structure correlates with hand posture and use in hominoids

Bone is capable of adapting during life in response to stress. Therefore, variation in locomotor and manipulative behaviours across extant hominoids may be reflected in differences in trabecular bone structure. The hand is a promising region for trabecular analysis, as it is the direct contact between the individual and the environment and joint positions at peak loading vary amongst extant hominoids. Building upon traditional volume of interest-based analyses, we apply a whole-epiphysis analytical approach using high-resolution microtomographic scans of the hominoid third metacarpal to investigate whether trabecular structure reflects differences in hand posture and loading in knuckle-walking (Gorilla, Pan), suspensory (Pongo, Hylobates and Symphalangus) and manipulative (Homo) taxa. Additionally, a comparative phylogenetic method was used to analyse rates of evolutionary changes in trabecular parameters. Results demonstrate that trabecular bone volume distribution and regions of greatest stiffness (i.e., Young's modulus) correspond with predicted loading of the hand in each behavioural category. In suspensory and manipulative taxa, regions of high bone volume and greatest stiffness are concentrated on the palmar or distopalmar regions of the metacarpal head, whereas knuckle-walking taxa show greater bone volume and stiffness throughout the head, and particularly in the dorsal region; patterns that correspond with the highest predicted joint reaction forces. Trabecular structure in knuckle-walking taxa is characterised by high bone volume fraction and a high degree of anisotropy in contrast to the suspensory brachiators. Humans, in which the hand is used primarily for manipulation, have a low bone volume fraction and a variable degree of anisotropy. Finally, when trabecular parameters are mapped onto a molecular-based phylogeny, we show that the rates of change in trabecular structure vary across the hominoid clade. Our results support a link between inferred behaviour and trabecular structure in extant hominoids that can be informative for reconstructing behaviour in fossil primates

Metacarpophalangeal joint loads during bonobo locomotion: model predictions vs. proxies

The analysis of internal trabecular and cortical bone has been an informative tool for drawing inferences about behaviour in extant and fossil primate taxa. Within the hand, metacarpal bone architecture has been shown to correlate well with primate locomotion; however, the extent of morphological differences across taxa is unexpectedly small given the variability in hand use. One explanation for this observation is that the activity-related differences in the joint loads acting on the bone are simply smaller than estimated based on commonly used proxies (i.e. external loading and joint posture), which neglect the influence of muscle forces. In this study, experimental data and a musculoskeletal finger model are used to test this hypothesis by comparing differences between climbing and knuckle-walking locomotion of captive bonobos (Pan paniscus) based on (i) joint load magnitude and direction predicted by the models and (ii) proxy estimations. The results showed that the activity-related differences in predicted joint loads are indeed much smaller than the proxies would suggest, with joint load magnitudes being almost identical between the two locomotor modes. Differences in joint load directions were smaller but still evident, indicating that joint load directions might be a more robust indicator of variation in hand use than joint load magnitudes. Overall, this study emphasizes the importance of including muscular forces in the interpretation of skeletal remains and promotes the use of musculoskeletal models for correct functional interpretations

A computational framework for canonical holistic morphometric analysis of trabecular bone

Bone is a remarkable, living tissue that functionally adapts to external loading. Therefore, bone shape and internal structure carry information relevant to many disciplines, including medicine, forensic science, and anthropology. However, morphometric comparisons of homologous regions across different individuals or groups are still challenging. In this study, two methods were combined to quantify such differences: (1) Holistic morphometric analysis (HMA) was used to quantify morphometric values in each bone, (2) which could then be mapped to a volumetric mesh of a canonical bone created by a statistical free-form deformation model (SDM). Required parameters for this canonical holistic morphometric analysis (cHMA) method were identified and the robustness of the method was evaluated. The robustness studies showed that the SDM converged after one to two iterations, had only a marginal bias towards the chosen starting image, and could handle large shape differences seen in bones of different species. Case studies were performed on metacarpal bones and proximal femora of different primate species to confirm prior study results. The differences between species could be visualised and statistically analysed in both case studies. cHMA provides a framework for performing quantitative comparisons of different morphometric quantities across individuals or groups. These comparisons facilitate investigation of the relationship between spatial morphometric variations and function or pathology, or both

Trabecular bone patterning across the human hand

Hand bone morphology is regularly used to link particular hominin species with behaviors relevant to cognitive/technological progress. Debates about the functional significance of differing hominin hand bone morphologies tend to rely on establishing phylogenetic relationships and/or inferring behavior from epigenetic variation arising from mechanical loading and adaptive bone modeling. Most research focuses on variation in cortical bone structure, but additional information about hand function may be provided through the analysis of internal trabecular structure. While primate hand bone trabecular structure is known to vary in ways that are consistent with expected joint loading differences during manipulation and locomotion, no study exists that has documented this variation across the numerous bones of the hand. We quantify the trabecular structure in 22 bones of the human hand (early/extant modern Homo sapiens) and compare structural variation between two groups associated with post-agricultural/industrial (post-Neolithic) and foraging/hunter-gatherer (forager) subsistence strategies. We (1) establish trabecular bone volume fraction (BV/TV), modulus (E), degree of anisotropy (DA), mean trabecular thickness (Tb.Th) and spacing (Tb.Sp); (2) visualize the average distribution of site-specific BV/TV for each bone; and (3) examine if the variation in trabecular structure is consistent with expected joint loading differences among the regions of the hand and between the groups. Results indicate similar distributions of trabecular bone in both groups, with those of the forager sample presenting higher BV/TV, E, and lower DA, suggesting greater and more variable loading during manipulation. We find indications of higher loading along the ulnar side of the forager sample hand, with high site-specific BV/TV distributions among the carpals that are suggestive of high loading while the wrist moves through the ‘dart-thrower's’ motion. These results support the use of trabecular structure to infer behavior and have direct implications for refining our understanding of human hand evolution and fossil hominin hand use

Musculoskeletal models of a human and bonobo finger: parameter identification and comparison to in vitro experiments

Introduction: Knowledge of internal finger loading during human and non-human primate activities such as tool use or knuckle-walking has become increasingly important to reconstruct the behaviour of fossil hominins based on bone morphology. Musculoskeletal models have proven useful for predicting these internal loads during human activities, but load predictions for non-human primate activities are missing due to a lack of suitable finger models. The main goal of this study was to implement both a human and a representative non-human primate finger model to facilitate comparative studies on metacarpal bone loading. To ensure that the model predictions are sufficiently accurate, the specific goals were: (1) to identify species-specific model parameters based on in vitro measured fingertip forces resulting from single tendon loading and (2) to evaluate the model accuracy of predicted fingertip forces and net metacarpal bone loading in a different loading scenario. Materials & Methods: Three human and one bonobo (Pan paniscus) fingers were tested in vitro using a previously developed experimental setup. The cadaveric fingers were positioned in four static postures and load was applied by attaching weights to the tendons of the finger muscles. For parameter identification, fingertip forces were measured by loading each tendon individually in each posture. For the evaluation of model accuracy, the extrinsic flexor muscles were loaded simultaneously and both the fingertip force and net metacarpal bone force were measured. The finger models were implemented using custom Python scripts. Initial parameters were taken from literature for the human model and own dissection data for the bonobo model. Optimized model parameters were identified by minimizing the error between predicted and experimentally measured fingertip forces. Fingertip forces and net metacarpal bone loading in the combined loading scenario were predicted using the optimized models and the remaining error with respect to the experimental data was evaluated. Results. The parameter identification procedure led to minor model adjustments but considerably reduced the error in the predicted fingertip forces (root mean square error reduced from 0.53/0.69 N to 0.11/0.20 N for the human/bonobo model). Both models remained physiologically plausible after the parameter identification. In the combined loading scenario, fingertip and net metacarpal forces were predicted with average directional errors below 6◦ and magnitude errors below 12%. Conclusions. This study presents the first attempt to implement both a human and nonhuman primate finger model for comparative palaeoanthropological studies. The good agreement between predicted and experimental forces involving the action of extrinsic flexors—which are most relevant for forceful grasping—shows that the models are likely sufficiently accurate for comparisons of internal loads occurring during human and non-human primate manual activities

The deep trabecular structure of first metacarpals in extant hominids

Objectives: Recent studies have associated subarticular trabecular bone distribution in the extant hominid first metacarpal (Mc1) with observed thumb use, to infer fossil hominin thumb use. Here, we analyze the entire Mc1 to test for interspecific differencesin: (1) the absolute volume of trabecular volume fraction, (2) the distribution ofthe deeper trabecular network, and (3) the distribution of trabeculae in the medullarycavity, especially beneath the Mc1 disto-radial flange. Materials and Methods: Trabecular bone was imaged using micro-computed tomography in a sample of Homo sapiens (n = 11), Pan paniscus (n = 10), Pan troglodytes(n = 11), Gorilla gorilla (n = 10) and Pongo sp., (n = 7). Using Canonical Holistic Morphometric Analysis (cHMA), we tested for interspecific differences in the trabecular bone volume fraction (BV/TV) and its relative distribution (rBV/TV) throughout the Mc1, including within the head, medullary cavity, and base. Results: P. paniscus had the highest, and H. sapiens the lowest, BV/TV relative to other species. rBV/TV distribution statistically distinguished the radial concentrations and lack of medullary trabecular bone in the H. sapiens Mc1 from all other hominids. H. sapiens and, to a lesser extent, G. gorilla also had a significantly higher trabecular volume beneath the disto-radial flange relative to other hominids. Discussion: These results are consistent with differences in observed thumb use in these species and may also reflect systemic differences in bone volume fraction. The trabecular bone extension into the medullary cavity and concentrations beneath the disto-radial flange may represent crucial biomechanical signals that will aid in the inference of fossil hominin thumb use

Trabecular architecture of the distal femur in extant hominids

Extant great apes are characterized by a wide range of locomotor, postural and manipulative behaviours that each require the limbs to be used in different ways. In addition to external bone morphology, comparative investigation of trabecular bone, which (re‐)models to reflect loads incurred during life, can provide novel insights into bone functional adaptation. Here, we use canonical holistic morphometric analysis (cHMA) to analyse the trabecular morphology in the distal femoral epiphysis of Homo sapiens (n = 26), Gorilla gorilla (n = 14), Pan troglodytes (n = 15) and Pongo sp. (n = 9). We test two predictions: (1) that differing locomotor behaviours will be reflected in differing trabecular architecture of the distal femur across Homo, Pan, Gorilla and Pongo; (2) that trabecular architecture will significantly differ between male and female Gorilla due to their different levels of arboreality but not between male and female Pan or Homo based on previous studies of locomotor behaviours. Results indicate that trabecular architecture differs among extant great apes based on their locomotor repertoires. The relative bone volume and degree of anisotropy patterns found reflect habitual use of extended knee postures during bipedalism in Homo, and habitual use of flexed knee posture during terrestrial and arboreal locomotion in Pan and Gorilla. Trabecular architecture in Pongo is consistent with a highly mobile knee joint that may vary in posture from extension to full flexion. Within Gorilla, trabecular architecture suggests a different loading of knee in extension/flexion between females and males, but no sex differences were found in Pan or Homo, supporting our predictions. Inter‐ and intra‐specific variation in trabecular architecture of distal femur provides a comparative context to interpret knee postures and, in turn, locomotor behaviours in fossil hominins

Effects of anti-resorptive treatment on the material properties of individual canine trabeculae in cyclic tensile tests

Osteoporosis is defined as a decrease of bone mass and strength, as well as an increase in fracture risk. It is conventionally treated with antiresorptive drugs, such as bisphosphonates (BPs) and selective estrogen receptor modulators (SERMs). Although both drug types successfully decrease the risk of bone fractures, their effect on bone mass and strength is different. For instance, BP treatment causes an increase of bone mass, stiffness and strength of whole bones, whereas SERM treatment causes only small (4%) increases of bone mass, but increased bone toughness. Such improved mechanical behavior of whole bones can be potentially related to the bone mass, bone structure or material changes. While bone mass and architecture have already been investigated previously, little is known about the mechanical behavior at the tissue/material level, especially of trabecular bone. As such, the goal of the work presented here was to fill this gap by performing cyclic tensile tests in a wet, close to physiologic environment of individual trabeculae retrieved from the vertebrae of beagle dogs treated with alendronate (a BP), raloxifene (a SERM) or without treatments. Identification of material properties was performed with a previously developed rheological model and of mechanical properties via fitting of envelope curves. Additionally, tissue mineral density (TMD) and microdamage formation were analyzed. Alendronate treatment resulted in a higher trabecular tissue stiffness and strength, associated with higher levels of TMD. In contrast, raloxifene treatment caused a higher trabecular toughness, pre-dominantly in the post-yield region. Microdamage formation during testing was not affected by either anti-resorptive treatment regimens. These findings highlight that the improved mechanical behavior of whole bones after anti-resorptive treatment is at least partly caused by improved material properties, with different mechanisms for alendronate and raloxifene. This study further shows the power of performing a mechanical characterization of trabecular bone at the level of individual trabeculae for better understanding of clinically relevant mechanical behavior of bone

Trabecular architecture in the thumb of Pan and Homo: implications for investigating hand use, loading, and hand preference in the fossil record

Objectives: Humans display an 85–95% cross-cultural right-hand bias in skilled tasks, which is considered a derived behavior because such a high frequency is not reported in wild non-human primates. Handedness is generally considered to be an evolutionary byproduct of selection for manual dexterity and augmented visuo-cognitive capabilities within the context of complex stone tool manufacture/use. Testing this hypothesis requires an understanding of when appreciable levels of right dominant behavior entered the fossil record. Because bone remodels in vivo, skeletal asymmetries are thought to reflect greater mechanical loading on the dominant side, but incomplete preservation of external morphology and ambiguities about past loading environments complicate interpretations. We test if internal trabecular bone is capable of providing additional information by analyzing the thumb of Homo sapiens and Pan. Materials and methods: We assess trabecular structure at the distal head and proximal base of paired (left/right) first metacarpals using micro-CT scans of Homo sapiens (n?=?14) and Pan (n?=?9). Throughout each epiphysis we quantify average and local bone volume fraction (BV/TV), degree of anisotropy (DA), and elastic modulus (E) to address bone volume patterning and directional asymmetry. Results: We find a right directional asymmetry in H. sapiens consistent with population-level handedness, but also report a left directional asymmetry in Pan that may be the result of postural and/or locomotor loading. Conclusion: We conclude that trabecular bone is capable of detecting right/left directional asymmetry, but suggest coupling studies of internal structure with analyses of other skeletal elements and cortical bone prior to applications in the fossil record

Inverse remodelling algorithm identifies habitual manual activities of primates based on metacarpal bone architecture

Previously, a micro-finite element (micro-FE)-based inverse remodelling method was presented in the literature that reconstructs the loading history of a bone based on its architecture alone. Despite promising preliminary results, it remains unclear whether this method is sensitive enough to detect differences of bone loading related to pathologies or habitual activities. The goal of this study was to test the sensitivity of the inverse remodelling method by predicting joint loading histories of metacarpal bones of species with similar anatomy but clearly distinct habitual hand use. Three groups of habitual hand use were defined using the most representative primate species: manipulation (human), suspensory locomotion (orangutan), and knuckle-walking locomotion (bonobo, chimpanzee, gorilla). Nine to ten micro-computed tomography scans of each species ( n=48 in total) were used to create micro-FE models of the metacarpal head region. The most probable joint loading history was predicted by optimally scaling six load cases representing joint postures ranging from −75∘ (extension) to +75∘ (flexion). Predicted mean joint load directions were significantly different between knuckle-walking and non-knuckle-walking groups ( p<0.05 ) and in line with expected primary hand postures. Mean joint load magnitudes tended to be larger in species using their hands for locomotion compared to species using them for manipulation. In conclusion, this study shows that the micro-FE-based inverse remodelling method is sensitive enough to detect differences of joint loading related to habitual manual activities of primates and might, therefore, be useful for palaeoanthropologists to reconstruct the behaviour of extinct species and for biomedical applications such as detecting pathological joint loading