The pattern of blood flow in the developing heart has long been proposed to play a significant role in cardiac morphogenesis. In response to flow-induced forces, cultured cardiac endothelial cells rearrange their cytoskeletal structure and change their gene expression profiles. To link such in vitro data to the intact heart, we performed quantitative in vivo analyses of intracardiac flow forces in zebrafish embryos. Using in vivo imaging, here we show the presence of high-shear, vortical flow at two key stages in the developing heart, and predict flow-induced forces much greater than might have been expected for micro-scale structures at low Reynolds numbers. To test the relevance of these shear forces in vivo, flow was occluded at either the cardiac inflow or outflow tracts, resulting in hearts with an abnormal third chamber, diminished looping and impaired valve formation. The similarity of these defects to those observed in some congenital heart diseases argues for the importance of intracardiac haemodynamics as a key epigenetic factor in embryonic cardiogenesis.
The embryonic vertebrate heart begins pumping blood long before the development of discernable chambers and valves. At these early stages, the heart tube has been described as a peristaltic pump. Recent advances in confocal laser scanning microscopy and four-dimensional visualization have warranted another look at early cardiac structure and function. We examined the movement of cells in the embryonic zebrafish heart tube and the flow of blood through the heart and obtained results that contradict peristalsis as a pumping mechanism in the embryonic heart. We propose a more likely explanation of early cardiac dynamics in which the pumping action results from suction due to elastic wave propagation in the heart tube.
SUMMARYThe hydrodynamic bases for the stability of locomotory motions in fishes are poorly understood, even for those fishes, such as the rigid-bodied smooth trunkfish Lactophrys triqueter, that exhibit unusually small amplitude recoil movements during rectilinear swimming. We have studied the role played by the bony carapace of the smooth trunkfish in generating trimming forces that self-correct for instabilities. The flow patterns, forces and moments on and around anatomically exact, smooth trunkfish models positioned at both pitching and yawing angles of attack were investigated using three methods: digital particle image velocimetry (DPIV), pressure distribution measurements, and force balance measurements. Models positioned at various pitching angles of attack within a flow tunnel produced well-developed counter-rotating vortices along the ventro-lateral keels. The vortices developed first at the anterior edges of the ventro-lateral keels,grew posteriorly along the carapace, and reached maximum circulation at the posterior edge of the carapace. The vortical flow increased in strength as pitching angles of attack deviated from 0°, and was located above the keels at positive angles of attack and below them at negative angles of attack. Variation of yawing angles of attack resulted in prominent dorsal and ventral vortices developing at far-field locations of the carapace; far-field vortices intensified posteriorly and as angles of attack deviated from 0°. Pressure distribution results were consistent with the DPIV findings, with areas of low pressure correlating well with regions of attached, concentrated vorticity. Lift coefficients of boxfish models were similar to lift coefficients of delta wings, devices that also generate lift through vortex generation. Furthermore, nose-down and nose-up pitching moments about the center of mass were detected at positive and negative pitching angles of attack, respectively. The three complementary experimental approaches all indicate that the carapace of the smooth trunkfish effectively generates self-correcting forces for pitching and yawing motions — a characteristic that is advantageous for the highly variable velocity fields experienced by trunkfish in their complex aquatic environment. All important morphological features of the carapace contribute to producing the hydrodynamic stability of swimming trajectories in this species.
For years, biomechanical engineers have studied the physical forces involved in morphogenesis of the heart. In a parallel stream of research, molecular and developmental biologists have sought to identify the molecular pathways responsible for embryonic heart development. Recently, several studies have shown that these two avenues of research should be integrated to explain how genes expressed in the heart regulate early heart function and affect physical morphogenetic steps, as well as to conversely show how early heart function affects the expression of genes required for morphogenesis. This review combines the perspectives of biomechanical engineering and developmental biology to lay out an integrated view of the role of mechanical forces in heart development.
Boxfishes (family Ostraciidae) are tropical reef-dwelling marine bony fishes that have about three-fourths of their body length encased in a rigid bony test. As a result, almost all of their swimming movements derive from complex combinations of movements of their median and paired fins (MPF locomotion). In terms of both body design and swimming performance, they are among the most sophisticated examples known of naturally evolved vertebrate autonomous underwater vehicles. Quantitative studies of swimming performance, biomechanics, and energetics in one model species have shown that (i) they are surprisingly strong, fast swimmers with great endurance; (ii) classical descriptions of how they swim were incomplete: they swim at different speeds using three different gaits; (iii) they are unusually dynamically well controlled and stable during sustained and prolonged rectilinear swimming; and (iv) despite unusually high parasite (fuselage) drag, they show energetic costs of transport indistinguishable from those of much better streamlined fishes using body and caudal fin (BCF) swimming modes at similar water temperatures and over comparable ranges of swimming speeds. We summarize an analysis of these properties based on a dynamic model of swimming in these fishes. This model accounts for their control, stability, and efficiency in moving through the water at moderate speeds in terms of gait changes, of water-flow patterns over body surfaces, and of complex interactions of thrust vectors generated by fin movements.
Boxfishes (Teleostei: Ostraciidae) are rigid-body, multi-propulsor swimmers that exhibit unusually small amplitude recoil movements during rectilinear locomotion. Mechanisms producing the smooth swimming trajectories of these fishes are unknown, however. Therefore, we have studied the roles the bony carapaces of these fishes play in generating this dynamic stability. Features of the carapaces of four morphologically distinct species of boxfishes were measured, and anatomically-exact stereolithographic models of the boxfishes were constructed. Flow patterns around each model were investigated using three methods: 1) digital particle image velocimetry (DPIV), 2) pressure distribution measurements, and 3) force balance measurements. Significant differences in both cross-sectional and longitudinal carapace morphology were detected among the four species. However, results from the three interrelated approaches indicate that flow patterns around the various carapaces are remarkably similar. DPIV results revealed that the keels of all boxfishes generate strong longitudinal vortices that vary in strength and position with angle of attack. In areas where attached, concentrated vorticity was detected using DPIV, low pressure also was detected at the carapace surface using pressure sensors. Predictions of the effects of both observed vortical flow patterns and pressure distributions on the carapace were consistent with actual forces and moments measured using the force balance. Most notably, the three complementary experimental approaches consistently indicate that the ventral keels of all boxfishes, and in some species the dorsal keels as well, effectively generate self-correcting forces for pitching motions-a characteristic that is advantageous for the highly variable velocity fields in which these fishes reside.
The small size and optical transparency of zebrafish embryos and larvae greatly facilitate modern intravital microscopic phenotyping of these experimentally tractable laboratory animals. Neither the experimentally derived dose-response relationships for chemicals commonly used in the mounting of live fish larvae, nor their effect on the stress of the animal, are currently available in the research literature. This is particularly problematic for IACUCs attempting to maintain the highest ethical standards of animal care in the face of a recent spate in investigator-initiated requests to use embryonic zebrafish as experimental models. The authors address this issue by describing the dose-dependent efficacy of several commonly used chemical mounting treatments and their effect on one stress parameter, embryo heart rate. The results of this study empirically define, for the first time, effective, minimally stressful treatments for immobilization and in vivo visualization during early zebrafish development.
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