Research ArticleAPPLIED SCIENCE AND ENGINEERING

Low-power microelectronics embedded in live jellyfish enhance propulsion

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Science Advances  29 Jan 2020:
Vol. 6, no. 5, eaaz3194
DOI: 10.1126/sciadv.aaz3194
  • Fig. 1 A. aurita swim controller design.

    (A) Square wave signal generated by the swim controller with an amplitude (A) of 3.7 V and a pulse width (T) of 10 ms, set at frequencies (f) of 0.25, 0.38, 0.50, 0.62, 0.75, 0.88, and 1.00 Hz. (B) Swim controller components. Housing includes (i) a polypropylene cap with a wooden pin that embeds into the bell center, and (ii) a plastic film to waterproof the housing, both offset with stainless steel and cork weights to keep the device approximately neutrally buoyant. Microelectronics include (iii) a TinyLily mini-processor, (iv) lithium polymer battery, and (v) two platinum-tip electrodes with LEDs to visually indicate stimulation. (C) Fully assembled device, with the processor and battery encased in the housing. (D) Simplified schematics of A. aurita anatomy, highlighting the subumbrellar (top) and exumbrellar (bottom) surfaces, rhopalia, muscle ring, and circumferential muscle fiber orientation, oral arms, and gonads/gastric pouches. (E) Swim controller (inactive) embedded into a free-swimming jellyfish, bell oriented subumbrellar side up, with the wooden pin inserted into the manubrium and two electrodes embedded into the muscle and mesogleal tissue near the bell margin. Photo credits for (B), (C), and (E): Nicole W. Xu, Stanford University.

  • Fig. 2 Signal validation using visual tags and frequency spectra to track muscle contractions.

    (A) A. aurita medusae (n = 10, 8.0 to 10.0 cm in diameter) were placed subumbrellar surface up in a plate without seawater for constrained muscle stimulation experiments (electrode not shown). The image is inverted so that the bell and plate are white, and black areas are reflections of light from animal tissue and the plate. For clarity, the margin of the bell is outlined in a red dotted circle, and the oral arms are colorized in blue. Visible implant elastomer tags (shown as colored red dots within red circles) were injected around the margin, and one tag was tracked per video to calculate the tissue displacement as a surrogate for muscle contractions. Spatial tests to determine whether electrode location affected the spectra were conducted at four locations, labeled in red numbers: (1) adjacent to the gastric pouches, (2) midway between the gastric pouches and margin, (3) at the rhopalia, and (4) at the margin away from the rhopalia (see “Extended results” sections in Supplementary Text). All other tests were conducted at location 2. (B) Example tag displacement as a function of time for an animal without any external stimulus. The red line indicates the centroid displacement, with the error calculated from assuming a half-pixel uncertainty in finding the centroid of the tag in each image, over 25 s. Note the temporal variation of muscle contractions, including periods of regular pulses and successive rapid pulses. (C) Example tag displacement for an animal with an external stimulus of 0.25 Hz, with each stimulus visualized as a vertical black line. Although contractions regularly follow external stimuli, natural animal pulses also occur at low frequencies. Note, for example, the double pulse after one stimulus (t ≈ 12 s). (D) Example tag displacement for an animal with an external stimulus of 1.00 Hz, with each stimulus visualized as a vertical black line. The same time window (25 s) is shown for a fair comparison to the previous two plots. Contractions regularly follow external stimuli. (E) SSASs averaged for jellyfish without any external stimulus (n = 12 for 10 animals, i.e., 2 jellyfish had two replicate clips each). The red line indicates the mean of normalized SSAS for each replicate, with the SD in pink. The peak of the mean SSAS is at 0.16 Hz. The FWHM is 0.24 Hz. (F) Jellyfish response to an inactive electrode embedded (n = 14 for 10 animals, i.e., 4 jellyfish had two replicate clips each). The peak of the mean SSAS is at 0.18 Hz. The FWHM is 0.16 Hz. Using a two-sample t test of the peak frequencies for both groups, the difference between the two samples was statistically insignificant (P = 0.68). (G) Sample SSAS for an electrical stimulus at 1.00 Hz (n = 10 jellyfish for an input signal of 4.2 V and 4.0 ms). The peak frequency occurs at 1.02 Hz, within the 0.02 window used to calculate the SSAS. Note that the spectrum has a sharper peak at the frequency of interest (FWHM of 0.04 Hz), as opposed to a wider FWHM in (B) and (C), the cases without any external stimulus. (H) Contour map of the frequency response of muscle contractions to external electrical stimuli. Each vertical line of data (centered on white lines at 0.25, 0.50, 0.75, 1.00, 1.20, 1.50, and 2.00 Hz) represents the PSD at one electrical input frequency, with the number of jellyfish tested shown above. The colors correspond to the amplitude of the PSD, in which higher values are shown in yellow and lower values in blue. The solid red line represents a one-to-one input-output response, and the dashed red line represents the reported physiological limit according to the minimum absolute refractory period of A. aurita muscle (32). Responsive trials are defined by whether the peak frequencies in the PSD lie within a window of 0.06 Hz of the solid red curve. (I) Contour maps of the unresponsive trials. Higher frequencies up to 90.00 Hz were also tested with similar unresponsive PSDs. Photo credit for (A): Nicole W. Xu, Stanford University.

  • Fig. 3 Externally driven swimming can increase speeds up to 2.8 times.

    (A) Schematic of vertical free-swimming experiments. Jellyfish (n = 6, resting bell diameters d ranging from 13.0 to 19.0 cm) swam downward starting from rest in a 1.8 m × 0.9 m × 0.9 m artificial seawater tank. Videos were recorded using a single camera at 60 fps. (B) Swimming speeds and enhancement factors for swim controller frequencies at 0, 0.25, 0.38, 0.50, 0.62, 0.75, 0.88, and 1.00 Hz. Each animal is represented by a different color curve, and the size range per animal reflects changes in bell growth over time (experiments were conducted over several days). Normalized speeds (body diameters per second) are indicated on the right ordinate axis. The enhancement factor is defined as the normalized swimming speed scaled by the mean of the normalized 0-Hz speed (in the absence of stimulation, in which the swim controller is embedded but inactive).

  • Fig. 4 External power requirements of the biohybrid robotic jellyfish compared to other swimming robots in literature.

    Marker shapes illustrate the type of aquatic robot, from biological soft robots such as the medusoid and robotic ray made from rat cardiomyocytes seeded on silicon scaffolds (9, 10) to purely mechanical robots, including bioinspired robots (3, 7, 33, 34) and an AUV (35). Marker colors illustrate the type of propulsion, including medusan (jellyfish swimming), thunniform (fish swimming), rajiform (ray swimming), and propeller-driven (AUVs). The external power (from the 10-mAh battery in the swim controller) per mass of the biohybrid robot (comprising the animal and the microelectronic system) is plotted versus swimming speed as red crosses. For actual values and details on the calculations, see table S3.

  • Fig. 5 Metabolic rate experiments.

    To determine the metabolic rate of jellyfish, oxygen concentrations were measured in animal tissue and the surrounding water and then converted into energy expenditure. (A) Experimental setup to measure bulk dissolved oxygen concentrations (in the water). Animals were placed subumbrellar surface upward in a sealed glass dish filled with 2 liters of artificial seawater, with two electrodes for frequency-driven cases. Oxygen levels in the water were measured using a MicroOptode oxygen probe. (B) Experimental setup to measure intragel oxygen concentrations (in the tissue). Animals were placed subumbrellar surface upward in a sealed glass dish filled with 2 liters of artificial seawater, with two electrodes for frequency-driven cases. Intragel oxygen levels were measured using a MicroOptode oxygen probe embedded into the tissue. (C) Representative plot of oxygen concentrations over time, measured from the MicroOptode. This example shows measurements of bulk oxygen levels in the water surrounding an animal with a swim controller–driven frequency of 1.00 Hz. Individual data points are shown in black, the best-fit line is shown in dark blue, and the SD is shown in the light blue shaded region. (D) Oxygen consumption rates of the surrounding water (dark blue), within animal tissue (light blue), and total (sum of the water and tissue measurements, purple) were calculated over a 6- to 8-hour period (n = 7 animals).

  • Fig. 6 Animal COT.

    The mean and SD of COT values (plotted in black) were calculated using experimental data from metabolic rate experiments and free-swimming speed experiments at 0 Hz (without the swim controller) and 0.25, 0.50, and 0.88 Hz (with the active swim controller). The experimentally calculated COT at 0 Hz is labeled as the baseline (horizontal black dashed line). The baseline values match experimental data reported in literature for A. aurita, in blue (1). Triangular markers indicate model estimates of COT. Values plotted in red were calculated assuming a cubic relationship between power and speed, using experimental data from free-swimming experiments (but no metabolic data). Values plotted in orange were calculated from a mechanistic model, adapted from literature (no experimental data) (20, 42).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/6/5/eaaz3194/DC1

    Supplementary Text

    Fig. S1. Muscle orientation along the subumbrellar surface.

    Fig. S2. Details of the adapted hydrodynamic model.

    Fig. S3. Parametric dependencies of enhanced propulsion.

    Fig. S4. Additional parametric dependencies of enhanced propulsion model parameter sweeps.

    Fig. S5. Power requirements of the microelectronic system versus animal.

    Table S1. Experimental parameters (columns) for each electrical signal characteristic test (rows).

    Table S2. Model parameters, including the resting body diameter (dr), range of diameters between relaxation and contraction geometries (Δd), resting body height (hr), range of height between contraction and relaxation geometries (Δd), tissue height or depth (hj), contraction time (tc), relaxation time (tr), and a geometric scale factor (s) that factors into each geometric parameter proportionally.

    Table S3. External power per mass calculations of various robotic constructs.

    Movie S1. A comparison of bell geometries for unstimulated swimming with an inactive swim controller embedded (left) and externally controlled swimming at 0.50 Hz (middle) and 0.88 Hz (right).

    References (43)

  • Supplementary Materials

    The PDFset includes:

    • Supplementary Text
    • Fig. S1. Muscle orientation along the subumbrellar surface.
    • Fig. S2. Details of the adapted hydrodynamic model.
    • Fig. S3. Parametric dependencies of enhanced propulsion.
    • Fig. S4. Additional parametric dependencies of enhanced propulsion model parameter sweeps.
    • Fig. S5. Power requirements of the microelectronic system versus animal.
    • Table S1. Experimental parameters (columns) for each electrical signal characteristic test (rows).
    • Table S2. Model parameters, including the resting body diameter (dr), range of diameters between relaxation and contraction geometries (Δd), resting body height (hr), range of height between contraction and relaxation geometries (Δd), tissue height or depth (hj), contraction time (tc), relaxation time (tr), and a geometric scale factor (s) that factors into each geometric parameter proportionally.
    • Table S3. External power per mass calculations of various robotic constructs.
    • Legend for movies S1
    • References (43)

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mov format). A comparison of bell geometries for unstimulated swimming with an inactive swim controller embedded (left) and externally controlled swimming at 0.50 Hz (middle) and 0.88 Hz (right).

     

    Correction (5 March 2020): An earlier version contained typographical and plotting errors related to literature and the theoretical models that were applied to measurement data. The main text, Fig. 4-6, and supplementary materials were updated.

    The original version is accessible here.

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