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BMC Bioinformatics
2013 Feb 01;14:37. doi: 10.1186/1471-2105-14-37.
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A novel application of motion analysis for detecting stress responses in embryos at different stages of development.
Tills O
,
Bitterli T
,
Culverhouse P
,
Spicer JI
,
Rundle S
.
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Motion analysis is one of the tools available to biologists to extract biologically relevant information from image datasets and has been applied to a diverse range of organisms. The application of motion analysis during early development presents a challenge, as embryos often exhibit complex, subtle and diverse movement patterns. A method of motion analysis able to holistically quantify complex embryonic movements could be a powerful tool for fields such as toxicology and developmental biology to investigate whole organism stress responses. Here we assessed whether motion analysis could be used to distinguish the effects of stressors on three early developmental stages of each of three species: (i) the zebrafish Danio rerio (stages 19 h, 21.5 h and 33 h exposed to 1.5% ethanol and a salinity of 5); (ii) the African clawed toad Xenopus laevis (stages 24, 32 and 34 exposed to a salinity of 20); and iii) the pond snail Radix balthica (stages E3, E4, E6, E9 and E11 exposed to salinities of 5, 10 and 15). Image sequences were analysed using Sparse Optic Flow and the resultant frame-to-frame motion parameters were analysed using Discrete Fourier Transform to quantify the distribution of energy at different frequencies. This spectral frequency dataset was then used to construct a Bray-Curtis similarity matrix and differences in movement patterns between embryos in this matrix were tested for using ANOSIM. Spectral frequency analysis of these motion parameters was able to distinguish stage-specific effects of environmental stressors in most cases, including Xenopus laevis at stages 24, 32 and 34 exposed to a salinity of 20, Danio rerio at 33 hpf exposed to 1.5% ethanol, and Radix balthica at stages E4, E9 and E11 exposed to salinities of 5, 10 and 15. This technique was better able to distinguish embryos exposed to stressors than analysis of manual quantification of movement and within species distinguished most of the developmental stages studied in the control treatments. This innovative use of motion analysis incorporates data quantifying embryonic movements at a range of frequencies and so provides an holistic analysis of an embryo's movement patterns. This technique has potential applications for quantifying embryonic responses to environmental stressors such as exposure to pharmaceuticals or pollutants, and also as an automated tool for developmental staging of embryos.
Figure 1. Optic flow of an E6 stage Radix balthica embryo showing angular rotations (red and yellow) and centre of mass (blue line).
Figure 2. Frame by frame optic flow parameters of control and treatment embryos for each of the developmental stages of Danio rerio, Xenopus laevis and Radix balthica. Red – positive angle movements, blue – negative angle movements, green – X coordinate of centre of mass, yellow – Y coordinate of centre of mass. A time period (Danio rerio – 10 min, Xenopus laevis – 10 min, Radix balthica – 5 min) of a single embryo is shown, exhibiting typical movement patterns for each treatment response per developmental stage.
Figure 3. Multidimensional scaling plots in two dimensions using Bray-Curtis similarity matrices. MDS plots using Bray-Curtis similarity matrices performed on logarithmically transformed spectral frequency data produced using Discrete Fourier Transform analysis of (i) negative angle (ii) positive angle (iii) centre of mass – rho and (iv) centre of mass – theta, frame-to-frame parameters for (a) Danio rerio, (b) Xenopus laevis and (c) Radix balthica under different environmental conditions and at different developmental stages. Bubble size represents the amount of tail flicks of Danio rerio and Xenopus laevis, the number of rotations of Radix balthica at stages E3, E4 and E6, and the number of complete gliding along the circumference of the egg capsule on stages E9 and E11.
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