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Biohybrid robot powered by an antagonistic pair of skeletal muscle tissues

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Science Robotics  30 May 2018:
Vol. 3, Issue 18, eaat4440
DOI: 10.1126/scirobotics.aat4440
  • Fig. 1 Construction of a biohybrid robot with an antagonistic pair of skeletal muscle tissues.

    (A) Illustrations of a biohybrid robot with an antagonistic pair of skeletal muscle tissues and bidirectional motion of the biohybrid robot by selective contractions of the skeletal muscle tissues. (B) An image of a myoblast-laden hydrogel sheet shaped with a PDMS stamp. (C) Construction of an antagonistic pair of skeletal muscle tissues by stacking and culturing the myoblast-laden hydrogel sheets on the skeleton in symmetrical positions. (D) Image of the biohybrid robot with the antagonistic pair of skeletal muscle tissues. Scale bars, 2 mm (B) and 5 mm (D).

  • Fig. 2 Properties of skeletal muscle tissues fabricated with myoblast-laden hydrogel sheets.

    (A) Short-axial sectional images (left and middle) and long-axial sectional images (right) of skeletal muscle tissues stained with H&E in our biohybrid robot. (B) Confocal images of the skeletal muscle tissues in the biohybrid robot with the following tissue immunostaining: cell nucleus (blue), α-actinin (red), and myosin heavy chain (green). (C) Temporal variation of contractile force of skeletal muscle tissues depending on the different electrical frequencies applied (electrical field, 1.5 V/mm; duration, 2 ms). (D) The p-p contractile force of different skeletal muscle tissues (n = 3) after changes in the applied electrical field (duration, 2 ms). (E) Changes in the p-p contractile force of different skeletal muscle tissues (n = 3) during culture (electrical field, 1.5 V/mm; duration, 2 ms). (F) Changes in the p-p contractile force of different skeletal muscle tissues fabricated using myoblast-laden hydrogel sheets with striped structures (n = 3) and those fabricated using myoblast-laden hydrogel blocks without the striped structures (n = 3) (electrical field, 1.5 V/mm; duration, 2 ms) (means ± SD). (G) Plots of the p-p contractile force of different skeletal muscle tissues (n = 3) relative to their length (the reference length is their culture length; electrical field, 1.5 V/mm; duration, 2 ms). (H) Plots of the passive force of different skeletal muscle tissues (n = 3) depending on their length. (A to D and F to H) Skeletal muscle tissues were cultured for 10 days after stacking the myoblast-laden hydrogel sheets. All error bars show SD. Scale bars, (A) 100 μm (left), 20 μm (middle), 50 μm (right); (B) 20 μm (left), 10 μm (right).

  • Fig. 3 Motions of the biohybrid robot powered by the antagonistic pair of skeletal muscle tissues.

    (A) Sequential images of the biohybrid robot when the skeletal muscle tissues were selectively contracted by applying electrical pulses (electrical field, 1.5 V/mm; frequency, 50 Hz; duration, 2 ms). (B and C) Changes of (B) the rotation angle of the joint and (C) the strain of the skeletal muscle tissues over time when the biohybrid robot was actuated by selectively applying electrical pulses (electrical field, 1.5 V/mm; frequency, 50 Hz; duration, 2 ms). (D and E) Range of (D) the rotation angle of the joint in different biohybrid robots (n = 4 to 7) and (E) the strain of each skeletal muscle tissue (n = 8 to 14) in different biohybrid robots during a single cycle of the bidirectional motion achieved by applying electrical pulses (duration, 2 ms). (F) Variation with time of the contractile length of one skeletal muscle tissue in different biohybrid robots (n = 4), that of skeletal muscle tissues on flexible substrates (n = 5), and that of free-standing skeletal muscle tissues (n = 4). Electrical pulses (electrical field, 1 V/mm; frequency, 1 Hz; duration, 2 ms) were applied to each tissue. Contractile lengths were normalized according to the contractile length at day 0 of each sample. *P < 0.01, unpaired t test. All error bars show SD. Scale bar, 5 mm.

  • Fig. 4 Object manipulations performed by our biohybrid robots.

    (A) Sequential images of a pick-and-place operation of the biohybrid robot by selective contractions of the skeletal muscle tissues generated with electrical pulses (electrical field, 1.5 V/mm; frequency, 50 Hz; duration, 2 ms). (B) Sequential images of picking up a square frame by the operation of two biohybrid robots. Skeletal muscle tissues were contracted selectively by applying electrical pulses (electrical field, 1.5 V/mm; frequency, 50 Hz; duration, 2 ms). Scale bars, 1 cm.

Supplementary Materials

  • robotics.sciencemag.org/cgi/content/full/3/18/eaat4440/DC1

    Section S1. Relationship between the motions of our biohybrid robot and the contractile properties of the skeletal muscle tissues

    Fig. S1. Fabrication process of our biohybrid robot.

    Fig. S2. Detailed process for stacking the myoblast-laden hydrogel sheets.

    Fig. S3. Formation of skeletal muscle tissue on our biohybrid robot.

    Fig. S4. Observation of our biohybrid robot.

    Fig. S5. Contractile properties of the striped patterned skeletal muscle tissues.

    Fig. S6. Confocal image of a skeletal muscle tissue immunostained with α-actinin, myogenin, and the cell nucleus.

    Fig. S7. Schematic illustration for comparison of a myoblast-laden hydrogel block and a stack of myoblast-laden hydrogel sheets.

    Fig. S8. Selective contractions of the skeletal muscle tissue in the biohybrid robot.

    Fig. S9. Variation with time of the motions of our biohybrid robot, a conventional biohybrid robot, and a free-standing single skeletal muscle tissue.

    Fig. S10. Calculated balance between the flexor muscle and extensor muscle.

    Movie S1. Bidirectional motions of our biohybrid robot.

    Movie S2. Motions of our biohybrid robot under applied electrical pulses (50 Hz, 2 ms) with different magnitudes of the electrical field.

    Movie S3. Pick-and-place operation by a single biohybrid robot.

    Movie S4. Pick-up operation achieved by two biohybrid robots.

  • Supplementary Materials

    Supplementary Material for:

    Biohybrid robot powered by an antagonistic pair of skeletal muscle tissues

    Yuya Morimoto, Hiroaki Onoe, Shoji Takeuchi*

    *Corresponding author. Email: takeuchi{at}iis.u-tokyo.ac.jp

    Published 30 May 2018, Sci. Robot. 3, eaat4440 (2018)
    DOI: 10.1126/scirobotics.aat4440

    This PDF file includes:

    • Section S1. Relationship between the motions of our biohybrid robot and the contractile properties of the skeletal muscle tissues
    • Fig. S1. Fabrication process of our biohybrid robot.
    • Fig. S2. Detailed process for stacking the myoblast-laden hydrogel sheets.
    • Fig. S3. Formation of skeletal muscle tissue on our biohybrid robot.
    • Fig. S4. Observation of our biohybrid robot.
    • Fig. S5. Contractile properties of the striped patterned skeletal muscle tissues.
    • Fig. S6. Confocal image of a skeletal muscle tissue immunostained with α-actinin, myogenin, and the cell nucleus.
    • Fig. S7. Schematic illustration for comparison of a myoblast-laden hydrogel block and a stack of myoblast-laden hydrogel sheets.
    • Fig. S8. Selective contractions of the skeletal muscle tissue in the biohybrid robot.
    • Fig. S9. Variation with time of the motions of our biohybrid robot, a conventional biohybrid robot, and a free-standing single skeletal muscle tissue.
    • Fig. S10. Calculated balance between the flexor muscle and extensor muscle.

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    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mp4 format). Bidirectional motions of our biohybrid robot.
    • Movie S2 (.mp4 format). Motions of our biohybrid robot under applied electrical pulses (50 Hz, 2 ms) with different magnitudes of the electrical field.
    • Movie S3 (.mp4 format). Pick-and-place operation by a single biohybrid robot.
    • Movie S4 (.mp4 format). Pick-up operation achieved by two biohybrid robots.

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