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Upconverting microgauges reveal intraluminal force dynamics in vivo

Nature volume 637, pages 76–83 (2025)Cite this article

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Abstract

The forces generated by action potentials in muscle cells shuttle blood, food and waste products throughout the luminal structures of the body. Although non-invasive electrophysiological techniques exist1,2,3, most mechanosensors cannot access luminal structures non-invasively4,5,6. Here we introduce non-toxic ingestible mechanosensors to enable the quantitative study of luminal forces and apply them to study feeding in living Caenorhabditis elegans roundworms. These optical ‘microgauges’ comprise upconverting NaY0.8Yb0.18Er0.02F4@NaYF4 nanoparticles embedded in polystyrene microspheres. Combining optical microscopy and atomic force microscopy to study microgauges in vitro, we show that force evokes a linear and hysteresis-free change in the ratio of emitted red to green light. With fluorescence imaging and non-invasive electrophysiology, we show that adult C. elegans generate bite forces during feeding on the order of 10 µN and that the temporal pattern of force generation is aligned with muscle activity in the feeding organ. Moreover, the bite force we measure corresponds to Hertzian contact stresses in the pressure range used to lyse the bacterial food of the worm7,8. Microgauges have the potential to enable quantitative studies that investigate how neuromuscular stresses are affected by ageing, genetic mutations and drug treatments in this organ and other luminal organs.

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Fig. 1: Synthesis of biocompatible microgauges compatible with passive ingestion.
Fig. 2: Caenorhabditis elegans ingest biocompatible microgauges.
Fig. 3: Optical mechanosensitivity is calibrated using confocal AFM.
Fig. 4: Microgauges enable simultaneous electrophysiology and optical mechanical imaging of feeding forces in live worms.

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Data availability

Source data for Figs. 1–4 are available at the Stanford Digital Repository service (https://doi.org/10.25740/ff923hb3417). All other source data are available upon reasonable request.

Code availability

The code used to extract ratiometric data from fluorescence spectra and segment images relies on prebuilt MATLAB functions and is available upon request.

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Acknowledgements

J.R.C. and A.S. acknowledge financial support from the National Science Foundation (NSF) through the Graduate Research Fellowships Program. J.A.D. is a Chan Zuckerberg Biohub – San Francisco Investigator and acknowledges funding from the Chan Zuckerberg Biohub San Francisco, as well as from the National Institutes of Health (NIH) under grant no. 1DPAI15207201 and from the NSF under grant no. 1933624. M.B.G. acknowledges funding from the NIH under grant no. R35NS105092. C.A.M. acknowledges funding from the Wu Tsai Neurosciences Institute at Stanford University. C. Siefe received support from an Eastman Kodak fellowship. C. Shi acknowledges funding from a US Navy NDSEG Fellowship under BAA #N00014-22-S-B001. X.W.G. and A.P. acknowledge financial support from the Army Research Office under grant no. W911NF2020171. A.P.’s time for reviewing and editing the written manuscript was supported under the auspices of the US Department of Energy by the Lawrence Livermore National Laboratory (LLNL) under contract DE-AC52-07NA27344 (LLNL review and release number LLNL-JRNL-854745-DRAFT). TEM/SEM imaging was performed at the Stanford Nano Shared Facilities (SNSF), supported by the National Science Foundation under award ECCS-2026822. This work would not have been possible without technical support from Z. Liao. We also thank B. Myers and A. Jayich for providing the confocal MATLAB code, H. Ji for consultations on data analysis, B. Ogulande for acquiring the Raman spectrum, M. Cano for counting worm progeny and R. Chen for suggesting the use of 4-dimethylaminopyridine.

Author information

Authors and Affiliations

  1. Department of Materials Science and Engineering, Stanford University, Stanford, CA, USA

    Jason R. Casar, Claire A. McLellan, Cindy Shi, Ariel Stiber, Chris Siefe, Abhinav Parakh, Malaya Gaerlan & Jennifer A. Dionne

  2. Department of Applied Physics, Stanford University, Stanford, CA, USA

    Alice Lay

  3. Materials Engineering Division, Lawrence Livermore National Laboratory, Livermore, CA, USA

    Abhinav Parakh

  4. Department of Biology, Stanford University, Stanford, CA, USA

    Malaya Gaerlan

  5. Department of Mechanical Engineering, Stanford University, Stanford, CA, USA

    X. Wendy Gu

  6. Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA, USA

    Miriam B. Goodman

  7. Department of Radiology, Stanford University, Stanford, CA, USA

    Jennifer A. Dionne

  8. Chan Zuckerberg Biohub, San Francisco, San Francisco, CA, USA

    Jennifer A. Dionne

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Contributions

All authors contributed to the review and editing of the manuscript text and figures. J.R.C. synthesized microgauges; collected data for the mechano-optical calibration, biocompatibility and worm-imaging experiments; and drafted the figures and text of the manuscript. C.A.M. constructed the confocal atomic force microscope. C. Shi assisted in the collection of mechano-optical data, worm-imaging data and SEM/TEM images, as well as nanoparticle synthesis. A.S. assisted in the collection of worm-imaging data and SEM/TEM images, as well as aqueous nanoparticle dispersal. A.L. devised and partially constructed the worm-imaging experimental set-up and assisted in nanoparticle synthesis. C. Siefe assisted in the collection of mechano-optical data and nanoparticle synthesis. A.P. and X.W.G. loaded the DAC. M.G. assisted in the worm-imaging experiments and the creation of schematics in Fig. 4. M.B.G. provided materials, reagents and expertise necessary for all worm-related work and optical/electrical data processing. J.A.D. provided materials, reagents and expertise necessary for the synthesis and characterization of microgauges and expertise in the construction and execution of optical microscopy, spectroscopy and AFM experiments. M.B.G. and J.A.D. conceived the idea and supervised the work. All authors contributed to interpreting the data and editing the manuscript.

Corresponding authors

Correspondence to Jason R. Casar, Miriam B. Goodman or Jennifer A. Dionne.

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The authors declare no competing interests.

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Nature thanks Xiaogang Liu, Andries Meijerink, Fan Zhang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Microgauge size measured via SEM.

a, A SEM micrograph of a monolayer of uncoated microgauges on silicon. Scale bar, 3 um. b, The distribution of N = 202 microgauge diameters (mean ± s.d. = 935 ± 367 nm), repeated for clarity from Fig. 1b).

Extended Data Fig. 2 The effect of sensor size on pharyngeal accumulation efficiency.

a, An SEM micrograph of microgauges on E. coli for size comparison. b, A TEM micrograph of a microgauge. TEM micrographs of core@shell NaY0.8Yb0.18Er0.02F4@NaYF4 UCNPs c, before and d, after wrapping with PMAO. Wrapped nanoparticles were dropcast from water. A series of bright field images of levamisole-treated worms after one-hour incubation with e, microgauges or f, singly dispersed PMAO-wrapped UCNPs. Scale bars are each 100 µm. False-colored UCL images (cyan) of the boxed pharyngeal regions are displayed in the inset of each picture, when applicable. Inset scale bars are each 20 µm each. The anterior of each animal is to the left.

Extended Data Fig. 3 Microgauge monolayers before and after melting.

a, An SEM micrograph of microgauge monolayers on hydrophilized silicon. Scale bar, 50 um. b, The same region after melting (30 minutes), with a higher resolution inset to show nanoparticles distributed evenly across the surface. Scale bars, 10 um, 500 nm (inset). Clusters like the one shown in the bottom left of the inset were easily visible from confocal UCL maps and were avoided during the calibration.

Extended Data Fig. 4 Er-Polystyrene energy overlap.

a, A simplified energy diagram of Er3+ that summarizes matrix quenching. Solid lines indicate radiative transitions, and dotted lines indicate non-radiative Energy Transfer (ET) to the aliphatic (gray and purple) and aromatic (yellow) C-H stretching modes on polystyrene. The corresponding Raman spectrum for polystyrene microbeads without nanoparticles at room temperature and ambient pressure (right). b, Raman spectrum for silicone oil (room temperature, ambient pressure). c, Raman spectra of polystyrene microbeads and silicone oil between ambient pressure (top) and 3.1 GPa (bottom). Fitted curves are filled in using the same color scheme as in panels a and b. P-Al1, P-Al2 and S-Al1, too close to deconvolve at all pressures, are fitted to a single peak. Thick vertical lines indicate the centers of mass of the red quenching 4F9/2 → 4I9/2 (2858 cm−1) and green quenching 4S3/2 → 4F9/2 transitions (3150 cm−1), respectively (values obtained for LaF3 from Carnall et al.60). Smaller red and green (circular end cap) colored lines above the spectra indicate the transition energies between individual stark levels that are above and below the centers of mass, respectively. Values in cm−1 are as follows; RQT: 2871, 2904, 2912, 2924, 2941, 2992, 2994, 3038, 3046, 3075, 3128; GQT: 3030, 3059, 3083, 3112, 3112, 3120, 3141 (obtained LaF3 for from Carnall et al.60). d, Peak energy (dots) and 2x standard deviations (colored area) of the fitted gaussian. Dotted black lines are the respective linear fits of the peak energies with pressure.

Extended Data Fig. 5 Ired:Igreen increases with (quasi)hydrostatic pressure.

a, Two spectra taken at either end of the pressure ramp showing the increase in relative red emission at high pressure. Both spectra are normalized to their respective green emission peaks. Inset, a schematic of the setup, wherein microgauges are compressed between two diamond culets. b, Ratiometric emission changes across three consecutive force loading-unloading cycles between ambient (0.0001 GPa) and high (5.8 GPa) pressure. The black line is the best fit line calculated in c, where all ratiometric changes are plotted versus pressure regardless of loading or unloading status. d, The corresponding background corrected red (left axis, red) and green (right axis, green) UCL intensities as a function of pressure.

Supplementary information

Supplementary Information

This file contains Supplementary Sections 1–8, including Supplementary Figs. 1–16 and additional references.

Supplementary Video 1

Microgauge cross-sections. Internal cross-sections of a microgauge taken in a focused ion beam scanning electron microscope after platinum deposition (outer white layer). The polystyrene appears black and the UCNPs embedded inside appear as white dots.

Supplementary Video 2

Microgauge transport under pharyngeal pumping. A video (66 fps) of microgauge transport under the influence of pharyngeal pumping in the terminal bulb. Dual illumination from a lamp (above) and a 980 nm laser (below) was used to make both the pharynx and the microgauges visible. Microgauge UCL is false coloured in cyan. Scale bar, 50 μm.

Supplementary Video 3

Microgauge ingestion in a freely crawling worm. A worm crawling on a lawn of microgauges and E. coli ingesting material and transporting it through the pharyngeal lumen to the intestines. The pharynx is facing in the direction of movement. Video has been slowed down 2.5 times. Scale bar, 250 μm.

Supplementary Video 4

Microgauge defecation in a freely crawling worm. A worm crawling on a lawn of microgauges and E. coli undergoing a single defecation motor programme cycle to expel material. Material can be seen moving anteriorly under the influence of a posterior body contraction then posteriorly under the influence of an anterior body contraction before the sphincter muscle rapidly and briefly contracts to expel material. The pharynx is facing left for the duration of the video. Video has been slowed down 2.5 times. Scale bar, 250 μm.

Supplementary Video 5

Microgauge defecation in a channel immobilized worm. A UCL video (10×, 50 fps, 2 s duration) of microgauge transport in the posterior intestinal lumen under the action of the defecation motor programme. The approximate onset of posterior body contraction (pBoc), anterior body contraction (aBoc) and expulsion (Exp) events are labelled in the appropriate frames. Scale bar, 50 μm.

Supplementary Video 6

Full segmentation example. A red UCL video (50×, 50 fps, 60 s duration) of microgauges during pharyngeal pumping. The outline indicates the bounds of the pixel segment used to calculate the optical time series. This is the same dataset used to calculate the event-triggered averages shown in Fig. 4c (iv). We note that, out of the 30 pumps identified from the corresponding EPG, only 12 had noise levels low enough to meet our quality control standards (see Supplementary Fig. 16 for those that did not). Scale bar, 20 μm.

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Casar, J.R., McLellan, C.A., Shi, C. et al. Upconverting microgauges reveal intraluminal force dynamics in vivo. Nature 637, 76–83 (2025). https://doi.org/10.1038/s41586-024-08331-x

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