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Imaging dynamic three-dimensional traction stresses.

ABSTRACT: Traction stress between contact objects is ubiquitous and crucial for various physical, biological, and engineering processes such as momentum transfer, tactile perception, and mechanical reliability. Newly developed techniques including electronic skin or traction force microscopy enable traction stress measurement. However, measuring the three-dimensional distribution during a dynamic process remains challenging. Here, we demonstrated a method based on stereo vision to measure three-dimensional traction stress with high spatial and temporal resolution. It showed the ability to image the two-stage adhesion failure of bionic microarrays and display the contribution of elastic resistance and adhesive traction to rolling friction at different contact regions. It also revealed the distributed sucking and sealing effect of the concavity pedal waves that propelled a snail crawling in the horizontal, vertical, and upside-down directions. We expected that the method would advance the understanding of various interfacial phenomena and greatly benefit related applications across physics, biology, and robotics.

SUBMITTER: Li Y

PROVIDER: S-EPMC8926338 | biostudies-literature | 2022 Mar

REPOSITORIES: biostudies-literature

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Imaging dynamic three-dimensional traction stresses.

Li Yuanzhe Y Bai Pengpeng P Cao Hui H Li Lvzhou L Li Xinxin X Hou Xin X Fang Jingbo J Li Jingyang J Meng Yonggang Y Ma Liran L Tian Yu Y

Science advances 20220316 11

Traction stress between contact objects is ubiquitous and crucial for various physical, biological, and engineering processes such as momentum transfer, tactile perception, and mechanical reliability. Newly developed techniques including electronic skin or traction force microscopy enable traction stress measurement. However, measuring the three-dimensional distribution during a dynamic process remains challenging. Here, we demonstrated a method based on stereo vision to measure three-dimensiona ...[more]

PMID: 35294236

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Project description:Tractions exerted by cells on their surroundings play an important role in many biological processes including stem cell differentiation, tumorigenesis, cell migration, cancer metastasis, and angiogenesis. The ability to quantify these tractions is important in understanding and manipulating these processes. Three-dimensional traction force microscopy (3DTFM) provides reliable means of evaluating cellular tractions by first measuring the displacement of fluorescent beads in response to these tractions in the surrounding matrix, and then using this measurement to compute the tractions. However, most applications of 3DTFM assume that the surrounding extra-cellular matrix (ECM) is non-fibrous, despite the fact that in many natural and synthetic environments the ECM contains a significant proportion of fibrous components. Motivated by this, we develop a computational approach for determining tractions, while accounting for the fibrous nature of the ECM. In particular, we make use of a fiber-based constitutive model in which the stress contains contributions from a distribution of nonlinear elastic fibers and a hyperelastic matrix. We solve an inverse problem with the nodal values of the traction vector as unknowns, and minimize the difference between a predicted displacement field, obtained by solving the equations of equilibrium in conjunction with the fiber-based constitutive model, and the measured displacement field at the bead locations. We employ a gradient-based minimization method to solve this problem and determine the gradient efficiently by solving for the appropriate adjoint field. We apply this algorithm to problems with experimentally observed cell geometries and synthetic, albeit realistic, traction fields to gauge its sensitivity to noise, and quantify the impact of using an incorrect constitutive model: the so-called model error. We conclude that the approach is robust to noise, yielding about 10% error in tractions for 5% displacement noise. We also conclude that the impact of model error is significant, where using a nonlinear exponential hyperelastic model instead of the fiber-based model, can lead to more than 100% error in the traction field. These results underline the importance of using appropriate constitutive models in 3DTFM, especially in fibrous ECM constructs.

Project description:Dynamic bone histomorphometry is the standard method for measuring bone remodeling at the level of individual events. Although dynamic bone histomorphometry is an invaluable tool for understanding osteoporosis and other metabolic bone diseases, the technique's two-dimensional nature requires the use of stereology and prevents measures of individual remodeling event number and size. Here, we used a novel three-dimensional fluorescence imaging technique to achieve measures of individual resorption cavities and formation events. We performed this three-dimensional histomorphometry approach using a common model of postmenopausal osteoporosis, the ovariectomized rat. The three-dimensional images demonstrated the spatial relationship between resorption cavities and formation events consistent with the hemiosteonal model of cancellous bone remodeling. Established ovariectomy was associated with significant increases in the number of resorption cavities per unit bone surface (2.38 ± 0.24 mm⁻² sham surgery versus 3.86 ± 0.35 mm⁻² bilateral ovariectomy [OVX], mean ± SD, p < 0.05) and total volume occupied by cavities per unit bone volume (0.38% ± 0.06% sham versus 1.12% ± 0.18% OVX, p < 0.001), but there was no difference in surface area per resorption cavity, maximum cavity depth, or cavity volume. In addition, we found that established ovariectomy is associated with increased size of bone formation events because of the merging of formation events (23,700 ± 6,890 µm² sham verusus 33,300 ± 7,950 µm² OVX). No differences in mineral apposition rate (determined in 3D) were associated with established ovariectomy. That established estrogen depletion is associated with increased number of remodeling events with only subtle changes in remodeling event size suggests that circulating estrogens may have their primary effect on the origination of new basic multicellular units with relatively little effect on the progression and termination of active remodeling events.

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Imaging dynamic three-dimensional traction stresses.

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Imaging dynamic three-dimensional traction stresses.

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