Ultrasound-activated ciliary bands for microrobotic systems inspired by starfish

Cilia, short hair-like appendages, are prevalent in biological systems, expertly manipulating fluids at viscosity-dominated regimes. Inspired by these natural systems, synthetic cilia have found applications in microfluidics and microrobotics for propulsion, pumping, mixing, and particle manipulation. Existing artificial cilia are often driven by electric, magnetic, light, or pressure fields. Magnetic actuation is popular due to its simplicity, while other methods include electrostatic, light-driven, and pneumatically-controlled actuators. Research on collective ciliary behavior, particularly metachronal waves in ciliary carpets, is growing, but most studies are numerical. Natural swimmers, such as starfish larvae, offer inspiration. Starfish larvae precisely adjust ciliary band orientation to control liquid flow, creating fluid sources and sinks for propulsion and feeding. This research focuses on ultrasound-activated ciliary bands, an area that has received limited attention despite ultrasound's widespread use in microfluidics and biomedical applications. The study aims to demonstrate controlled liquid flow generation using ultrasound-actuated synthetic ciliary bands, leveraging nonlinear acoustics and source/sink arrangements for microscale propulsion and biomimetic particle trapping.

The paper reviews existing artificial cilia actuation methods, including magnetic, electrostatic, light-driven, and pneumatic approaches. It highlights the growing interest in understanding the collective behavior of cilia arrays and metachronal waves. The authors note that most studies have been numerical, and engineered ciliary bands typically produce simple unidirectional flow. The authors cite existing research on the use of magnetic cilia carpets for fluid transport and numerical studies of collective ciliary behavior. They emphasize the lack of diversity in ciliary band designs and hydrodynamic functions, contrasting this with the intricate flow control observed in nature, particularly in starfish larvae. The paper also mentions the limited exploration of acoustically-activated cilia for liquid pumping and the lack of research on the interaction of multiple cilia in ciliary bands. Finally, it emphasizes the advantages of ultrasound-based ciliary bands for biomedical applications, such as their safety, non-invasiveness, and deep tissue penetration.

The researchers fabricated + and − ciliary band arrangements using UV photopolymerization. This one-step high-throughput method involved UV light polymerization of a polyethylene glycol and photo-initiator solution sandwiched between glass slides, using masks containing the ciliary band designs. Each cilium had a length of approximately 100 µm, a base thickness of 15–35 µm, and a height of 50 µm. The ciliary bands were placed in an acoustic chamber with a liquid solution containing tracer particles. A piezo transducer generated the acoustic field, and the setup was mounted on an inverted microscope for observation using high-speed cameras. The excitation frequency was modulated from 20–100 kHz with an applied power of 1–25 V peak-to-peak (Vpp). Particle image velocimetry (PIV) was used to measure flow velocities. Numerical simulations were also conducted using COMSOL Multiphysics to model the acoustic streaming patterns, utilizing a perturbation approach to solve the first-order harmonic and second-order steady fields. The simulations solved the first-order system for the acoustic response, using a time-harmonic solution, and then used the solution to determine the forcing terms for the second-order system which represented the time-averaged response. Experiments were performed on a Zeiss Axiovert 200 M inverted microscope equipped with fluorescent and high-speed cameras, and video analysis was done using ImageJ and MATLAB software. The fabrication process involved a custom-built projection UV photolithography system using a UV lamp, an inverted microscope, photomasks, and a photosensitive polymer mixture containing photo-cross-linkable polyethylene glycols (PEGs), a photo-initiator, and fluorescent dyes.

The + ciliary band configuration generated an outward flow, acting as a fluid source, while the − configuration created an inward flow, behaving as a fluid sink. Particle transport analysis revealed velocities up to 10 mm/s near cilium tips. The flow field for both configurations exhibited counter-rotating vortices. The streaming velocity was shown to scale quadratically with the applied voltage. Numerical simulations reproduced the experimental flow patterns. A bio-inspired microrobot, with + and − ciliary bands on opposite sides, demonstrated left-to-right translational propulsion at approximately 2.6 mm/s. The microrobot's propulsion was explained by the balanced forces along its long axis and the unbalanced forces along its short axis. Despite the system operating in a viscous-dominated regime (Reynolds number ≈ 0.7), propulsion was achieved due to the high-frequency actuation (frequency Reynolds number ≈ 31.4–62.8), introducing sufficient inertia to overcome the scallop theorem. Control experiments showed that propulsion was directly attributable to the ciliary bands, and not the background acoustic field. A microparticle trapping mechanism was demonstrated by placing + and − ciliary bands adjacent to each other, mimicking the starfish larva's feeding mechanism. Particles were transported from the + to − band, with transport efficiency tunable by adjusting the acoustic field intensity.

The findings demonstrate successful fabrication and characterization of ultrasound-activated ciliary bands that generate controlled fluid flow. The ability to create both fluid sources and sinks using different ciliary orientations provides a foundation for building more complex microfluidic devices and microrobots. The successful demonstration of propulsion in a viscous-dominated regime, despite the reciprocal motion of the cilia, highlights the importance of the high-frequency actuation. The biomimetic microparticle trapping mechanism offers potential applications in lab-on-a-chip technologies for particle manipulation. The study's success in achieving microscale propulsion using reciprocal motion via high-frequency ultrasound actuation provides an innovative approach to designing microrobots, bypassing limitations imposed by the scallop theorem.

This research successfully demonstrated ultrasound-activated synthetic ciliary bands that can generate controlled fluid flow and enable microscale propulsion and particle trapping. The design principles presented offer a new approach for building microrobotic systems, circumventing the scallop theorem using high-frequency actuation. Future work will focus on incorporating magnetic particles for combined ultrasound and magnetic control, developing hybrid ciliary bands with microbubbles for frequency-based control, investigating multi-microrobot interactions, and exploring applications in biological environments.

The current study focuses on a fixed ciliary band angle. Future work will explore dynamically changing ciliary orientations. While the trapping mechanism is demonstrated, future studies should investigate the simultaneous trapping and transport of particles during propulsion. The study primarily uses water; future work needs to explore performance in more complex biological fluids such as blood.