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Nat Commun
2021 Nov 09;121:6455. doi: 10.1038/s41467-021-26607-y.
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Ultrasound-activated ciliary bands for microrobotic systems inspired by starfish.
Dillinger C
,
Nama N
,
Ahmed D
.
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Cilia are short, hair-like appendages ubiquitous in various biological systems, which have evolved to manipulate and gather food in liquids at regimes where viscosity dominates inertia. Inspired by these natural systems, synthetic cilia have been developed and utilized in microfluidics and microrobotics to achieve functionalities such as propulsion, liquid pumping and mixing, and particle manipulation. Here, we demonstrate ultrasound-activated synthetic ciliary bands that mimic the natural arrangements of ciliary bands on the surface of starfish larva. Our system leverages nonlinear acoustics at microscales to drive bulk fluid motion via acoustically actuated small-amplitude oscillations of synthetic cilia. By arranging the planar ciliary bands angled towards (+) or away (-) from each other, we achieve bulk fluid motion akin to a flow source or sink. We further combine these flow characteristics with a physical principle to circumvent the scallop theorem and realize acoustic-based propulsion at microscales. Finally, inspired by the feeding mechanism of a starfish larva, we demonstrate an analogous microparticle trap by arranging + and - ciliary bands adjacent to each other.
Fig. 1. Starfish larva-inspired ultrasound ciliary band designs.a A starfish larva exhibits a complex flow profile of counter-rotating vortices generated by a series of + and − ciliary bands arranged on its body protuberances. Inset: (top) A + ciliary band comprises a pair of angled ciliary arrays that face each other and causes the liquid to flow away on a plane perpendicular to the center of the ciliary band. (Bottom) A − ciliary band consists of two ciliary arrays oriented away from each other and directs the liquid flow to the center of the band. b A starfish-inspired microrobot consisting of a + (top) and a − (bottom) ciliary band placed in a tracer solution. The ciliary bands oscillate when actuated by ultrasound, producing complex flow profiles similar to those observed with its biological counterpart. Scale bar, 250 μm.
Fig. 2. Tangential flow along angled ciliary array when exposed to ultrasound.a Image sequences (at t = 0.000–0.067 s) demonstrate ~6 μm tracer particles, indicated by red, green, and blue lines, traveling along one cilium tip to the next from right-to-left in the direction the tips are angled at excitation frequency and amplitude of 33.7 kHz and 5 VPP, respectively (see also Supplementary Movie 2). Due to residual non-polymerized and sticky polymer material on the surface of individual cilia and in between located web-like structures, tracers adhere to the structure’s surface. b Velocity analysis of the tracers (Source Data 1 and Supplementary Software 1), along the horizontal axis of the image sequences in a, revealed a cyclic acceleration/deceleration pattern. Particles reached maximum speeds when they approached a ciliary tip, followed by a deceleration phase. Scale bar, 50 μm.
Fig. 3. Experimental, characterization, and numerical demonstration of bioinspired ultrasound ciliary bands (Supplementary Movie 4).a PIV generated velocity fields of a + ciliary band that causes the liquid to flow away on a plane perpendicular to the center of the ciliary band at excitation frequency and amplitude of 68.7 kHz and 20 VPP, respectively. The inset indicates localized counter-rotating vortices at the innermost tips of the + ciliary band configuration. b PIV generated velocity fields of a − ciliary band, which directs the liquid flow to the center of the band at 68.8 kHz and 22 VPP, respectively. The inset indicates localized counter-rotating vortices at the innermost tips of the − ciliary band configuration. Plots of average velocities of c. + and d. − ciliary bands at sites indicated by magenta boxes in a and b versus voltage applied. The particles immersed in water transport at a speed proportional to the square of the voltage applied and this quadratic relation is reasonably well satisfied as indicated by the log plots. In each data point, 150−400 velocity measurements are averaged and the standard deviation is calculated and they are represented as black error bars (Source Data 2 and Supplementary Software 2). Numerical simulation of microstreaming using perturbation approach of e + ciliary band and f − ciliary band. The insets indicate numerically calculated counter-rotating vortices at the innermost tips of the respective ciliary band configuration. Color bars represent normalized streaming velocities. Scale bar, 100 μm.
Fig. 4. Propulsion of bioinspired ultrasound microrobot.a Schematic of an artificial microrobot consisting of a – ciliary band on the left and a + ciliary band on the right. Red and blue arrows indicate tangential and vertical velocity, respectively. b Superimposed time-lapse image (time is advancing in the direction of the blue arrow at the values given below) of controlled translation motion of a microrobot at excitation frequency and amplitude of 68.8 kHz and 20 VPP, respectively (see also Supplementary Movie 6). c Image sequence illustrating the streaming flow profile of the bioinspired microrobot. A stack of 150 images was used; the video was captured using a high-speed camera at a framerate of 1069 fps (see also Supplementary Movie 7). d PIV generated velocity fields demonstrate the complex flow behavior developed in the surrounding liquid. Minimum and maximum flow velocities are marked by red and blue regions, respectively. Scale bars, 250 μm.
Fig. 5. Bioinspired microparticle trapping using a combination of + and – ciliary bands.a Schematic of a bioinspired trapping mechanism consisting of a + ciliary band adjacent to a – ciliary band (see also Supplementary Movie 8). b Image sequence demonstrating microparticles becoming trapped in the – ciliary band, as indicated by red, green, and blue trajectories at 68.5 kHz and 20 VPP. c Expanded spatial trajectories of microparticles that became trapped by the flow field produced from the adjacent + and – ciliary bands. d Plots of microparticle velocity versus y-position: the left panel indicates the source and the right panel the sinking behavior of the trapping ciliary band (Source Data 3 and Supplementary Software 3). Scale bar, 200 μm.
Fig. 6. Acoustic power-dependent transport and trapping.Transport and trapping of 10 µm particles (colored trajectories) with maximum transport efficiencies of microparticles traveling from + to – ciliary band were achieved at a 12 and b 18 volts peak-to-peak (VPP). c The trapping mode became dominant as excitation (Supplementary Software 4). Scale bar, 200 μm.
