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      AutoBend: An Automated Approach for Estimating Intervertebral Joint Function from Bone-Only Digital Models

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      Integrative Organismal Biology

      Oxford University Press

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          Synopsis

          Deciphering the biological function of rare or extinct species is key to understanding evolutionary patterns across the tree of life. While soft tissues are vital determinants of joint function, they are rarely available for study. Therefore, extracting functional signals from skeletons, which are more widely available via museum collections, has become a priority for the field of comparative biomechanics. While most work has focused on the limb skeleton, the axial skeleton plays a critical role in body support, respiration, and locomotion, and is therefore of central importance for understanding broad-scale functional evolution. Here, we describe and experimentally validate AutoBend, an automated approach to estimating intervertebral joint function from bony vertebral columns. AutoBend calculates osteological range of motion (oROM) by automatically manipulating digitally articulated vertebrae while incorporating multiple constraints on motion, including both bony intersection and the role of soft tissues by restricting excessive strain in both centrum and zygapophyseal articulations. Using AutoBend and biomechanical data from cadaveric experiments on cats and tegus, we validate important modeling parameters required for oROM estimation, including the degree of zygapophyseal disarticulation, and the location of the center of rotation. Based on our validation, we apply a model with the center of rotation located within the vertebral disk, no joint translation, around 50% strain permitted in both zygapophyses and disks, and a small amount of vertebral intersection permitted. Our approach successfully reconstructs magnitudes and craniocaudal patterns of motion obtained from ex vivo experiments, supporting its potential utility. It also performs better than more typical methods that rely solely on bony intersection, emphasizing the importance of accounting for soft tissues. We estimated the sensitivity of the analyses to vertebral model construction by varying joint spacing, degree of overlap, and the impact of landmark placement. The effect of these factors was small relative to biological variation craniocaudally and between bending directions. We also present a new approach for estimating joint stiffness directly from oROM and morphometric measurements that can successfully reconstruct the craniocaudal patterns, but not magnitudes, derived from experimental data. Together, this work represents a significant step forward for understanding vertebral function in difficult-to-study (e.g., rare or extinct) species, paving the way for a broader understanding of patterns of functional evolution in the axial skeleton.

          Translated abstract

          Resumo [Portuguese] Decifrar a função biológica de espécies raras ou extintas é fundamental para se compreender os padrões evolutivos na árvore da vida. Embora os tecidos moles sejam determinantes vitais das funções articulares, estes raramente estão disponíveis para estudo. Portanto, extrair dados funcionais provenientes de esqueletos, que são mais amplamente disponíveis por meio de coleções de museus, tornou-se uma prioridade para o campo da biomecânica comparada. Embora a maioria dos trabalhos biomecânicos tenham focado no esqueleto apendicular, o esqueleto axial também desempenha um papel crítico para o suporte corporal, respiração e locomoção e, portanto, é de importância central para a compreensão da evolução funcional em escalas amplas. Nesse trabalho, nós descrevemos e validamos experimentalmente o AutoBend, uma abordagem automatizada para estimar a função da articulação intervertebral de colunas vertebrais ósseas. O AutoBend calcula a amplitude do movimento osteológico (AMO) manipulando automaticamente as vértebras reconstruídas digitalmente e incorporando várias restrições de movimento, incluindo restrições das interseções ósseas e o papel de restrição dos tecidos moles na tensão excessiva sobre as articulações dos centros vertebrais e zigapofisárias. Usando AutoBend e dados biomecânicos de experimentos cadavéricos em gatos e lagartos tegus, validamos parâmetros de modelagem importantes e necessários para as estimativa do AMO, incluindo o grau de desarticulação zigapofisária e a localização do centro de rotação. Com base nessa validação, aplicamos um modelo com o centro de rotação localizado dentro do disco vertebral, sem translação articular, com cerca de 50% de tensão permitida nas zigapófises e discos vertebrais, além de uma pequena quantidade de intersecção vertebral permitida. Nossa abordagem reconstrói com sucesso magnitudes e padrões de movimento craniocaudais obtidos a partir de experimentos ex vivo, corroborando a sua potencial utilidade. Esse modelo também tem um desempenho melhor do que os métodos mais típicos que dependem apenas das interseções ósseas, enfatizando a importância de se levar em conta o papel dos tecidos moles. Estimamos a sensibilidade das análises à reconstrução do modelo vertebral, variando o espaçamento entre articulações, o grau de sobreposição e o impacto da localização dos pontos de referência. O efeito desses fatores foi pequeno em relação à variação biológica craniocaudal e entre as direções de flexão. Apresentamos aqui também uma nova abordagem para se estimar a rigidez articular diretamente à partir do AMO e medidas morfométricas que podem reconstruir com sucesso os padrões craniocaudais (embora não as magnitudes) derivados de dados experimentais. Este trabalho representa um passo significativo para a melhor compreensão da função vertebral em espécies difíceis de estudar (por exemplo, raras ou extintas), abrindo caminho para uma compreensão mais ampla dos padrões de evolução funcional no esqueleto axial.

          Translated abstract

          Resumen [Spanish] Descifrar la función biológica de especies raras o extintas es fundamental para comprender los patrones evolutivos del árbol de la vida. Aunque los tejidos blandos son determinantes vitales de la función articular, raramente están disponibles para su estudio. Por lo tanto, la extracción de datos funcionales de esqueletos, que están más comumente disponibles a través de colecciones de museos, se ha convertido en una prioridad para el campo de la biomecánica comparada. Aunque la mayor parte del trabajo biomecánico se ha centrado en el esqueleto apendicular, el esqueleto axial también desempeña un papel fundamental para el soporte del cuerpo, la respiración y la locomoción y, por lo tanto, es de vital importancia para comprender la evolución funcional a gran escala. En este trabajo, describimos y validamos experimentalmente AutoBend, una herramienta automatizada para estimar la función de la articulación intervertebral en las columnas vertebrales óseas. AutoBend calcula el rango de movimiento osteológico (RMOo) manipulando automáticamente las vértebras reconstruidas digitalmente e incorporando varias restricciones de movimiento, incluidas las restricciones de intersección ósea y el papel de la restricción de tejidos blandos en la tensión excesiva sobre las articulaciones cigapofisarias y centros vertebrales. Utilizando AutoBend y datos biomecánicos de experimentos cadavéricos en gatos y lagartos tegus, validamos importantes parámetros de modelado necesarios para estimar el RMOo, incluido el grado de desarticulación cigapofisaria y la ubicación del centro de rotación. Con base en esta validación, aplicamos un modelo con el centro de rotación ubicado dentro del disco vertebral, sin traslación articular, con 50% de tensión permisible en la cigapófisis y los discos vertebrales, además de una pequeña cantidad de intersección vertebral permitida. Nuestra herramienta reconstruye con éxito magnitudes craneocaudales y patrones de movimiento obtenidos de experimentos ex vivo, corroborando su potencial utilidad. Este modelo también funciona mejor que los métodos más típicos que se basan solo en las intersecciones óseas, enfatizando la importancia de tener en cuenta el papel de los tejidos blandos. Estimamos la sensibilidad de los análisis a la reconstrucción del modelo vertebral, variando el espaciamiento entre articulaciones, el grado de superposición y el impacto de la ubicación de los puntos de referencia. El efecto de estos factores fue pequeño en relación a la variación biológica craneocaudal y entre las direcciones de flexión. También presentamos aquí un nuevo enfoque para estimar la rigidez articular directamente de la RMOo y mediciones morfométricas que pueden reconstruir con éxito los patrones craneocaudales (aunque no las magnitudes) derivados de datos experimentales. Este trabajo representa un paso significativo hacia una mejor comprensión de la función vertebral en especies difíciles de estudiar (por ejemplo, raras o extintas), allanando el camino para una comprensión más amplia de los patrones de evolución funcional en el esqueleto axial.

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          Most cited references 75

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          Re-epithelialization and immune cell behaviour in an ex vivo human skin model

          A large body of literature is available on wound healing in humans. Nonetheless, a standardized ex vivo wound model without disruption of the dermal compartment has not been put forward with compelling justification. Here, we present a novel wound model based on application of negative pressure and its effects for epidermal regeneration and immune cell behaviour. Importantly, the basement membrane remained intact after blister roof removal and keratinocytes were absent in the wounded area. Upon six days of culture, the wound was covered with one to three-cell thick K14+Ki67+ keratinocyte layers, indicating that proliferation and migration were involved in wound closure. After eight to twelve days, a multi-layered epidermis was formed expressing epidermal differentiation markers (K10, filaggrin, DSG-1, CDSN). Investigations about immune cell-specific manners revealed more T cells in the blister roof epidermis compared to normal epidermis. We identified several cell populations in blister roof epidermis and suction blister fluid that are absent in normal epidermis which correlated with their decrease in the dermis, indicating a dermal efflux upon negative pressure. Together, our model recapitulates the main features of epithelial wound regeneration, and can be applied for testing wound healing therapies and investigating underlying mechanisms.
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            Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation.

            The American sabercat Smilodon fatalis is among the most charismatic of fossil carnivores. Despite broad agreement that its extraordinary anatomy reflects unique hunting techniques, after >150 years of study, many questions remain concerning its predatory behavior. Were the "sabers" used to take down large prey? Were prey killed with an eviscerating bite to the abdomen? Was its bite powerful or weak compared with that of modern big cats? Here we quantitatively assess the sabercat's biomechanical performance using the most detailed computer reconstructions yet developed for the vertebrate skull. Our results demonstrate that bite force driven by jaw muscles was relatively weak in S. fatalis, one-third that of a lion (Panthera leo) of comparable size, and its skull was poorly optimized to resist the extrinsic loadings generated by struggling prey. Its skull is better optimized for bites on restrained prey where the bite is augmented by force from the cervical musculature. We conclude that prey were brought to ground and restrained before a killing bite, driven in large part by powerful cervical musculature. Because large prey is easier to restrain if its head is secured, the killing bite was most likely directed to the neck. We suggest that the more powerful jaw muscles of P. leo may be required for extended, asphyxiating bites and that the relatively low bite forces in S. fatalis might reflect its ability to kill large prey more quickly, avoiding the need for prolonged bites.
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              Three-dimensional limb joint mobility in the early tetrapod Ichthyostega.

              The origin of tetrapods and the transition from swimming to walking was a pivotal step in the evolution and diversification of terrestrial vertebrates. During this time, modifications of the limbs—particularly the specialization of joints and the structures that guide their motions—fundamentally changed the ways in which early tetrapods could move. Nonetheless, little is known about the functional consequences of limb anatomy in early tetrapods and how that anatomy influenced locomotion capabilities at this very critical stage in vertebrate evolution. Here we present a three-dimensional reconstruction of the iconic Devonian tetrapod Ichthyostega and a quantitative and comparative analysis of limb mobility in this early tetrapod. We show that Ichthyostega could not have employed typical tetrapod locomotory behaviours, such as lateral sequence walking. In particular, it lacked the necessary rotary motions in its limbs to push the body off the ground and move the limbs in an alternating sequence. Given that long-axis rotation was present in the fins of tetrapodomorph fishes, it seems that either early tetrapods evolved through an initial stage of restricted shoulder and hip joint mobility or that Ichthyostega was unique in this respect. We conclude that early tetrapods with the skeletal morphology and limb mobility of Ichthyostega were unlikely to have made some of the recently described Middle Devonian trackways.
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                Author and article information

                Contributors
                Journal
                Integr Org Biol
                Integr Org Biol
                iob
                Integrative Organismal Biology
                Oxford University Press
                2517-4843
                2021
                13 October 2021
                13 October 2021
                : 3
                : 1
                Affiliations
                Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University , 26 Oxford Street, Cambridge, MA 02138, USA
                Department of Earth and Environmental Sciences, University of Manchester , Williamson Building, Oxford Road, Manchester M13 9PL, UK
                Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University , 26 Oxford Street, Cambridge, MA 02138, USA
                Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University , 26 Oxford Street, Cambridge, MA 02138, USA
                Author notes
                Article
                obab026
                10.1093/iob/obab026
                8514422
                14b655c4-736a-4a15-8415-8220d4908fd1
                © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Pages: 21
                Product
                Funding
                Funded by: National Science Foundation, DOI 10.13039/100000001;
                Award ID: EAR-1524523
                Award ID: DEB-1757749
                Categories
                Article
                AcademicSubjects/SCI00960

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