Trabecular structure of the third metatarsal head distinguishes between a grasping and non-grasping foot

The human foot is unique compared to that of other extant apes in its adaptations for bipedal locomotion. At the metatarsophalangeal joint, bipedal locomotion in humans is associated with a high degree of dorsiflexion at toe-off and this more extreme joint position is reflected in the external morphology of the metatarsal head and base of the proximal pedal phalanx. These morphological features related to dorsiflexion of the toes have been used to determine human-like foot loading in fossil hominins, including dorsal doming of the metatarsal head and the presence of an associated sulcus, and dorsal canting of the proximal pedal phalangeal base [1]. However, the loading regime of the metatarsophalangeal joint in fossil hominins remains uncertain, due to the presence of more primitive traits, for example relatively long, highly curved proximal phalanges [2], morphologies that are also present among more recent hominins belonging to the genus Homo [3]. Phalanges with such a morphology indicate the potential importance of arboreal locomotion, using the foot to grasp branches for stability when navigating unstable arboreal supports. As the internal structure of bone adapts during an individual’s lifetime, it can provide additional information about loading of the metatarsophalangeal joints [4]. As such, trabecular structure of the third metatarsal head may provide signals of human-like toe off and of an ape-like grasping foot. To explore the relationship between locomotor behaviour and internal bone structure, we quantified trabecular bone of the third metatarsal head of Homo sapiens (n = 7), Pan troglodytes (n = 7) and Pongo pygmaeus (n = 4). Using medtool software (www.dr-pahr.at/medtool), 3D morphometric maps of the distribution of bone volume fraction (BV/TV) were generated, and BV/TV and degree of anisotropy (DA) were quantified. Results reveal that the trabecular bone structure of the third metatarsal head discriminates among bipedal humans, arboreal/terrestrial chimpanzees and arboreal orangutans. The distribution of BV/TV reflects loading of the human metatarsal head in dorsiflexion during toe-off and does not indicate loading of the plantar surface. In chimpanzees, in contrast to humans, a localisation of BV/TV across the entire surface of the metatarsal head suggests loading throughout the range of dorso-to-plantar flexion, likely due to a combination of terrestrial and arboreal locomotor modes. In orangutans, the region of highest BV/TV is located on the plantar surface, reflecting frequent use of the foot to grasp arboreal substrates. The human metatarsal head is characterised by a high DA reflecting the stereotypical loading regime of this joint during bipedal locomotion. As is characteristic of trabecular architecture across the skeleton of sedentary human populations, the human metatarsal head has a low BV/TV [5]. This human-typical signal may be due to lower overall activity levels. As the internal bone structure of the third metatarsal head reflects locomotor behaviour among these three extant taxa, it may further inform interpretations of foot use, both during toe-off and grasping, among early hominins. References:[1] Latimer, B., Lovejoy, C.O., 1990. Metatarsophalangeal joints of Australopithecus afarensis. American Journal of Physical Anthropology 83, 13-23.[2] Stern, J., Susman, R., 1983. The locomotor anatomy of Australopithecus afarensis. American Journal of Physical Anthropology 60, 279-317.[3] DeSilva, J., McNutt, E., Benoit, J., Zipfel, B., 2019. One small step: A review of Plio-Pleistocene hominin foot evolution. American Journal of Physical Anthropology 168:S67, 63-140.[4] Komza, K., Skinner, M.M., 2019. First metatarsal trabecular bone structure in extant hominoids and Swartkrans hominins. Journal of Human Evolution 131, 1-21.[5] Ryan, T.M., Shaw, C.N., 2015. Gracility of the modern Homo sapiens skeleton is the result of decreased biomechanical loading. Proceedings of the National Academy of Sciences of the United States of America 112, 372-377

Analyse micro-architecturale du développement de la marche bipède chez le jeune enfant

Lors du développement normal des jeunes enfants des populations actuelles, une marche bipède autonome (MBA) s’acquiert entre les âges de 9 et 18 mois. L’acquisition de cette étape clé du développement psychomoteur montre une variabilité dans les rythmes de sa mise en place qui est, pour une part importante, définie culturellement. Elle est précédée par la mise en place de stratégies alternatives de déplacement, comme la quadrupédie, et entraîne de nombreux changements cinétiques, cinématiques et anatomiques. Il est connu depuis longtemps que la microarchitecture de l’os trabéculaire (MAOT) répond aux changements biomécaniques. De plus, la métaphyse distale du radius, composante de l’articulation du poignet, est fortement sollicitée pendant le développement de la MBA, notamment pendant la période quadrupède. L’hypothèse est faite que la MAOT présente des variations directement liées à la mise en place de la MBA. Ainsi, huit métaphyses distales de radius d’enfants sains âgés de 0 à 3 ans, provenant de la collection de référence de Bologne, ont été microscannées à une résolution de 10,7 μm. L’analyse de ces images a permis de mesurer la fraction volumique osseuse (BV/TV), l’épaisseur, l’espacement et le facteur ellipsoïde trabéculaire (Tb.Th, Tb.Sp et Tb.EF) et d’extraire des cartes 3D de la répartition de l’os trabéculaire. Les résultats obtenus mettent en évidence des modifications importantes de la structure de l’os trabéculaire et de sa répartition entre 7 et 15 mois, période à laquelle quadrupédie et bipédie se succèdent. Ils permettent alors d’identifier comment la MAOT s’adapte aux changements biomécaniques propres à l’utilisation du poignet pendant cette transition locomotrice. L’analyse microarchitecturale de l’acquisition de la MBA donne ainsi d’importantes informations quant aux rythmes du développement des enfants, qui en termes évolutifs, permettraient de comprendre le développement psychomoteur dans les populations du passé et autorisent un lien direct entre biologie et culture

Trabecular Analysis of the Distal Radial Metaphysis during the Acquisition of Crawling and Bipedal Walking in Childhood: A Preliminary Study

In modern day populations, children following a normal pattern of development acquire independent bipedal locomotion between the ages of 9 and 18 months. Variability in the timing of this psychomotor developmental milestone depends on various factors, including cultural influences. It is well known that trabecular bone adapts to changes in biomechanical loading and that this can be influenced by alternative locomotor modes, such as crawling, which may be adopted before the acquisition of bipedal locomotion. With the onset of crawling, increased loading of the distal metaphysis of the radius, a component of the wrist, may lead to changes in trabecular bone architecture. To test this hypothesis, eight distal metaphyses of the radius of nonpathological children aged 0 to 3 years from the Bologna collection of identified skeletons were μCT-scanned at a resolution of 10.7 μm. The microarchitectural parameters of the trabecular bone (trabecular bone volume fraction, trabecular thickness, trabecular spacing, and trabecular ellipsoid factor) were quantified for the entire metaphysis and 3D morphometric maps of the distribution of the bone volume fraction were generated. Analysis of these microarchitectural parameters and the 3D morphometric maps show changes in the trabecular bone structure between 6 and 15 months, the period during which both crawling and bipedalism are acquired. This preliminary study analyzed the trabecular structure of the growing radius in three dimensions for the first time, and suggests that ontogenetic changes in the trabecular structure of the radial metaphysis may be related to changes in the biomechanical loading of the wrist during early locomotor transitions, i.e. the onset of crawling. Moreover, microarchitectural analysis could supply important information on the developmental timing of locomotor transitions, which would facilitate interpretations of locomotor development in past populations