Abstract
The ability to propel against flows, that is, to perform positive rheotaxis, can provide exciting opportunities for applications in targeted therapeutics and non-invasive surgery. So far no biocompatible technologies exist for navigating microparticles upstream when they are in a background fluid flow. Inspired by many naturally occurring microswimmers—such as bacteria, spermatozoa and plankton—that utilize the no-slip boundary conditions of the wall to exhibit upstream propulsion, here we report on the design and characterization of self-assembled microswarms that can execute upstream motility in a combination of external acoustic and magnetic fields. Both acoustic and magnetic fields are safe to humans, non-invasive, can penetrate deeply into the human body and are well-developed in clinical settings. The combination of both fields can overcome the limitations encountered by single actuation methods. The design criteria of the acoustically induced reaction force of the microswarms, which is needed to perform rolling-type motion, are discussed. We show quantitative agreement between experimental data and our model that captures the rolling behaviour. The upstream capability provides a design strategy for delivering small drug molecules to hard-to-reach sites and represents a fundamental step towards the realization of micro- and nanosystem navigation against the blood flow.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Rolling microswarms along acoustic virtual walls
Nature Communications Open Access 29 November 2022
-
Adaptive wireless millirobotic locomotion into distal vasculature
Nature Communications Open Access 01 August 2022
-
Multimodal microwheel swarms for targeting in three-dimensional networks
Scientific Reports Open Access 24 March 2022
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 per month
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$99.00 per year
only $8.25 per issue
Rent or buy this article
Get just this article for as long as you need it
$39.95
Prices may be subject to local taxes which are calculated during checkout





Data availability
The authors declare that data supporting the findings of this study are available within the paper and its Supplementary Information. Source data are provided with this paper.
References
Ashkin, A., Dziedzic, J. M., Bjorkholm, J. E. & Chu, S. Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11, 288–290 (1986).
Ma, F., Wang, S., Wu, D. T. & Wu, N. Electric-field induced assembly and propulsion of chiral colloidal clusters. Proc. Natl Acad. Sci. USA 112, 6307–6312 (2015).
Snezhko, A. & Aranson, I. S. Magnetic manipulation of self-assembled colloidal asters. Nat. Mater. 10, 698–703 (2011).
Lipfert, J., JKerssemakers, J. W. J. & Jager, T. Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA-DNA filaments. Nat. Methods 7, 977–980 (2010).
Sukhov, A. & Berakdar, J. Local control of ultrafast dynamics of magnetic nanoparticles. Phys. Rev. Lett. 102, 057204 (2009).
Miyashita, S., Guitron, S., Li, S. & Rus, D. Robotic metamorphosis by origami exoskeletons. Sci. Robot. 2, eaao4369 (2017).
Grifantini, R. et al. Magnetically driven drug delivery systems improving targeted immunotherapy for colon-rectal cancer. J. Control. Release 280, 76–86 (2018).
Yang, M. & Ripoll, M. Soft matter hydrodynamic simulations of self-phoretic microswimmers. Soft Matter. 10, 6208–6218 (2014).
Shi, J. et al. Acoustic tweezers: patterning cells and microparticles using standing surface acoustic waves (SSAW). Lab Chip 9, 2890–2895 (2009).
Ahmed, D. et al. Rotational manipulation of single cells and organisms using acoustic waves. Nat. Commun. 7, 11085 (2016).
Ding, X. et al. On-chip manipulation of single microparticles, cells, and organisms using surface acoustic waves. Proc. Natl Acad. Sci. USA 109, 11105–11109 (2012).
Friend, J. & Yeo, L. Y. Microscale acoustofluidics: microfluidics driven via acoustics and ultrasonics. Rev. Mod. Phys. 83, 647–704 (2011).
Purcell, E. M. Life at low Reynolds number. Am. J. Phys. 45, 3–11 (1977).
Williams, B. J., Anand, S. V., Rajagopalan, J. & Saif, M. T. A. A self-propelled biohybrid swimmer at low Reynolds number. Nat. Commun. 5, 3081 (2014).
Medina-Sánchez, M. & Schmidt, O. G. Medical microbots need better imaging and control. Nature 545, 406–408 (2017).
Lauga, E., Diluzio, W. R., Whitesides, G. M. & Stone, H. A. Swimming in circles: motion of bacteria near solid boundaries. Biophys. J. 90, 400–412 (2006).
Kaya, T. & Koser, H. Direct upstream motility in Escherichia coli bacteria preparation. Biophys. J. 102, 1514–1523 (2012).
Mattick, J. S. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56, 289–314 (2002).
Kantsler V., Dunkel J., Blayney M. & Goldstein R. E. Rheotaxis facilitates upstream navigation of mammalian sperm cells. eLife 3, e02403 (2014).
Miki, K. & Clapham, D. E. Article rheotaxis guides mammalian sperm. Curr. Biol. 23, 443–452 (2013).
Elgeti, J., Winkler, R. G. & Gompper, G. Physics of microswimmers—single particle motion and collective behavior. Rep. Prog. Phys. 78, 056601 (2014).
Durham, W. M. & Stocker, R. Thin phytoplankton layers: characteristics, mechanisms, and consequences. Annu. Rev. Mar. Sci. 4, 177–207 (2012).
Miki, K. & Clapham, D. E. Rheotaxis guides mammalian sperm. Curr. Biol. 23, 443–452 (2013).
Kaupp, U. B. & Strünker, T. Signaling in sperm: more dfferent than similar. Trends Cell Biol. 27, 101–109 (2017).
Simmchen, J. et al. Topographical pathways guide chemical microswimmers. Nat. Commun. 7, 10598 (2016).
Das, S. et al. Boundaries can steer active Janus spheres. Nat. Commun. 6, 8999 (2015).
Liu, C., Zhou, C., Wang, W. & Zhang, H. P. Bimetallic microswimmers speed up in confining channels. Phys. Rev. Lett. 117, 198001 (2016).
Katuri, J., Uspal, W. E., Simmchen, J., Miguel-lópez, A. & Sánchez, S. Cross-stream migration of active particles. Sci. Adv. 4, eaao1755 (2018).
Palacci, J.et al. Artificial rheotaxis. Sci. Adv. 1, –e1400214 (2015).
Palacci, J., Sacanna, S., Steinberg, A. P., Pine, D. J. & Chaikin, P. M. Living crystals of light-activated colloidal surfers. Science 339, 936–941 (2013).
Ren, L. et al. Rheotaxis of bimetallic micromotors driven by driven by chemical–acoustic hybrid power. ACS Nano. 11, 10591–10598 (2017).
De Ávila, B. E. et al. Micromotor-enabled active drug delivery for in vivo treatment of stomach infection Berta. Nat. Commun. 8, 272 (2017).
Tierno, P., Golestanian, R., Pagonabarraga, I. & Sague, F. Controlled swimming in confined fluids of magnetically actuated colloidal rotors. Phys. Rev. Lett. 101, 218304 (2008).
Martinez-pedrero, F., Ortiz-ambriz, A., Pagonabarraga, I. & Tierno, P. Colloidal microworms propelling via a cooperative hydrodynamic conveyor belt. Phys. Rev. Lett. 115, 138301 (2015).
Ahmed, D. et al. Neutrophil-inspired propulsion in a combined acoustic and magnetic field. Nat. Commun. 8, 770 (2017).
Shi, J., Ahmed, D., Mao, X., Lin, S. S. & Huang, T. J. Acoustic tweezers: patterning cells and microparticles using standing surface acoustic waves (SSAW). Lab Chip 9, 2890–2895 (2009).
Bruus, H. Acoustofluidics 7: the acoustic radiation force on small particles. Lab Chip 12, 1014–1021 (2012).
Bruus, H. Acoustofluidics 10: scaling laws in acoustophoresis. Lab Chip 12, 1578–1586 (2012).
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
Rune Barnkob, H. B., Iranmanesh, I., Wiklund, M. & Bruus, H. Measuring acoustic energy density in microchannel acoustophoresis using a simple and rapid light-intensity method. Lab Chip 12, 2337–2344 (2012).
Wei, W., Thiessen, D. B. & Marston, P. L. Acoustic radiation force on a compressible cylinder in a standing wave. J. Acoust. Soc. Am. 116, 201–208 (2004).
Garbin, A., Leibacher, I., Hahn, P. & Le Ferrand, H. Acoustophoresis of disk-shaped microparticles: a numerical and experimental study of acoustic radiation forces and torques. J. Acoust. Soc. Am. 138, 2759 (2015).
Klingenberg, D. J., Ulicny, J. C. & Golden, M. A. Mason numbers for magnetorheology. J. Rheol. 51, 883 (2017).
Sherman, S. G., Becnel, A. C. & Wereley, N. M. Relating Mason number to Bingham number in magnetorheological fluids. J. Magn. Magn. Mater. 380, 98–104 (2015).
Krishnamurthy, H. et al. Dynamics of rotating paramagnetic particle chains simulated by particle dynamics, Stokesian dynamics and lattice Boltzmann methods. Microfluid. Nanofluid. 5, 33–41 (2008).
Sherwood, J. D. Stokes drag on a disc with a Navier slip condition near a plane wall. Fluid Dyn. Res. 45, 055505 (2013).
Goldmans, A. J., Cox, R. G. & Brenner, H. Slow viscous motion of a sphere parallel to a plane wall—I motion through a quiescent fluid. Chem. Eng. Sci. 22, 637–651 (1967).
Krishnan, G. P. & Leighton, D. T. Inertial lift on a moving sphere in contact with a plane wall in a shear flow. Phys. Fluids. 7, 2538 (1995).
Wu, Y. H. Stokes drag on a disc with a Navier slip condition near a plane wall Stokes drag on a disc with a Navier slip condition near a plane wall. Fluid Dyn. Res. https://doi.org/10.1088/0169-5983/45/5/055505 (2013).
Filho, M. M. C. & Machado, J. C. The ultrasonic attenuation coefficient for human blood plasma in the frequency range of 7–90 MHz. Proc. IEEE Ultrason. Symp. 3, 2073–2077 (2004).
Coey, J. M. D. Magnetism and Magnetic Materials (Cambridge Univ. Press, 2010).
Medina-Sánchez, M. & Schmidt, O. G. Medical microbots need better imaging and control. Nature 545, 406–408 (2017).
Wu, Z. et al. A microrobotic system guided by photoacoustic computed tomography for targeted navigation in intestines in vivo. Sci. Robotics 4, eaax0613 (2019).
Awatani, J. Studies on acoustic radiation pressure. I. (General considerations). J. Acoust. Soc. Am. 27, 278–281 (1955).
Acknowledgements
This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme grant agreement no. 853309 (SONOBOTS) and grant agreement no. 743217 (SOMBOT). In addition, the work has been supported by ETH Zurich Career Seed Grant (grant no. 14 17-2) and DFG Priority Programme SPP 1726, Microswimmers—“From single particle motion to collective behaviour.”
Author information
Authors and Affiliations
Contributions
D.A. initiated, designed, and supervised the project. D.A contributed to the experimental design and scientific presentation. D.H., M.G., A.S. and D.A. performed all of the experiments and data analysis. A.S., D.R., D.A. and J.H. developed the theoretical studies. D.A. wrote the manuscript with contribution from all authors. All authors contributed to the scientific discussion.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1
Fabrication of the acoustofluidic device.
Extended Data Fig. 2 Ultrasound manipulation system.
(a) Schematic demonstrates the ultrasound particle manipulation setup. (b) A micrograph shows trapped microparticles in pressure nodes arrays when exposed to an ultrasound at ~2.1 MHz and 12 V, respectively.
Extended Data Fig. 3
Experimental setup of microparticle manipulation in acoustic and magnetic field.
Extended Data Fig. 4
An electromagnetic setup purchased from MagnebotiX AG (Zurich, Switzerland) with eight independently controlled coils was integrated with the inverted microscope to generate a rotating magnetic field.
Extended Data Fig. 5
Swarm stability against thermal fluctuation A plot demonstrates the ratio of the thermal to magnetic forces versus the radius of superparamagnetic particles. Magnetic forces dominate over the thermal effects for particles with radii 3 μm.
Extended Data Fig. 6
Poiseuille flow profile Experimental characterization of the Poiseuille flow profile within the circular channel.
Extended Data Fig. 7
Upstream motion Upstream migration of swarm of microparticles in a combined acoustic and magnetic field where the pressure node lies outside the capillary, see also Supplementary Movie 6.
Supplementary information
Supplementary Information
Supplementary Notes 1–5, Extended Data Figs. 1–7, Tables 1 and 2, legends for Supplementary Videos 1–9 and references.
Supplementary Video 1
Fluorescent microparticles getting trapped in the acoustic pressure nodes.
Supplementary Video 2
Acoustic switching of microparticles from the centre to the sidewall of the channel. Recorded at 15 fps and played at 60 fps.
Supplementary Video 3
An array of trapped microparticles was acoustically shifted. Recorded at 15 fps and played at 30 fps.
Supplementary Video 4
Formation of microswarms in an acoustic and magnetic field. The top panel shows microswarm configuration sandwiched between two glass slides and in the absence of an acoustic field. The middle panel shows microswarm structures in the acoustic pressure node. The bottom panel demonstrates microswarms formation in the pressure node when imposed upon an external flow field.
Supplementary Video 5
Recruitment of microswarm near a wall in the presence of an acoustic field.
Supplementary Video 6
Upstream migration of microparticles in a combined acoustic and magnetic field with the pressure node outside the capillary. Recorded at 15 fps and played at 60 fps.
Supplementary Video 7
Upstream migration of microparticles with the pressure node lies inside the capillary.
Supplementary Video 8
Deformation of the microswarm when the acoustic field is turned on and off.
Supplementary Video 9
Ultrasound manipulation of polystyrene particles (of 5.5 µm) under pulsatile flow. An external flow of 150 µl min–1 (corresponds to 200 mm s–1) with a periodic flow of 1 Hz is developed along a 1.55 mm outer diameter capillary. A pair of piezoelectric transducers were bonded across the channel and were actuated at 5.1 MHz, 20 VPP. The video is recorded at 7 fps and played at 15 fps.
Source data
Source Data Fig. 2
Source data for Fig. 2b,c.
Source Data Fig. 5
Source data for Fig. 5b,c.
Rights and permissions
About this article
Cite this article
Ahmed, D., Sukhov, A., Hauri, D. et al. Bioinspired acousto-magnetic microswarm robots with upstream motility. Nat Mach Intell 3, 116–124 (2021). https://doi.org/10.1038/s42256-020-00275-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s42256-020-00275-x
This article is cited by
-
Artificial microtubules for rapid and collective transport of magnetic microcargoes
Nature Machine Intelligence (2022)
-
Rolling microswarms along acoustic virtual walls
Nature Communications (2022)
-
Multimodal microwheel swarms for targeting in three-dimensional networks
Scientific Reports (2022)
-
Autonomous environment-adaptive microrobot swarm navigation enabled by deep learning-based real-time distribution planning
Nature Machine Intelligence (2022)
-
Adaptive wireless millirobotic locomotion into distal vasculature
Nature Communications (2022)