Synergistic photoactuation of bilayered spiropyran hydrogels for predictable origami-like shape change

•Bilayer hydrogels exhibit opposite volumetric change in response to light exposure•Coupling expanding and contracting layers generates synergistic bending with light•Constructs exhibit light-driven locomotion and origami-like 3D shape changes•Observed shape changes in designed constructs predicted by analytical modeling A grand challenge for materials science is the development of biomimetic soft matter that emulates behaviors of living creatures in response to an energy input. Photoresponsive hydrogels are particularly attractive in this context because they can expand or contract in response to light through reversible changes in molecular structure and internal water content. Using hydrogels developed recently in our laboratory, which expand with light exposure, and previously known ones that contract, we report here on the synergistic faster bending actuation of bilayered hydrogels with opposite response to light. We also show that constructs with chemically connected sequences of bilayer and photoinactive hydrogels undergo reversible and predictable origami-like 3D shape changes as well as unidirectional walking motion when exposed to light and dark periods. This work advances our ability to design molecularly life-like behavior in robotic soft materials responding to external stimuli. Development of stimuli-responsive soft matter that undergoes fast and reversible shape changes that mimic living organisms is a grand challenge for materials science. We report here on the molecular design of photoactive bilayer actuators that can rapidly respond to visible light, leading to complex but predictable bio-inspired shape changes. The mechanism of accelerated actuation is rooted in the simultaneous photoexpansion of one layer and photocontraction of the other triggered by the same light stimulus. The opposing response leads to a synergistic effect that results in fast bending actuation. The synergistic bilayers were bridged with light-inactive segments to generate macroscopic constructs capable of undergoing programmable 3D origami-like shape change upon irradiation. By controlling the anisotropic friction with the substrate, these constructs displayed unidirectional inchworm- and octopus-like locomotion over macroscopic distances. The soft matter systems investigated here demonstrate the possibility of molecularly engineering photoactuators that mimic functions we associate with living organisms. Development of stimuli-responsive soft matter that undergoes fast and reversible shape changes that mimic living organisms is a grand challenge for materials science. We report here on the molecular design of photoactive bilayer actuators that can rapidly respond to visible light, leading to complex but predictable bio-inspired shape changes. The mechanism of accelerated actuation is rooted in the simultaneous photoexpansion of one layer and photocontraction of the other triggered by the same light stimulus. The opposing response leads to a synergistic effect that results in fast bending actuation. The synergistic bilayers were bridged with light-inactive segments to generate macroscopic constructs capable of undergoing programmable 3D origami-like shape change upon irradiation. By controlling the anisotropic friction with the substrate, these constructs displayed unidirectional inchworm- and octopus-like locomotion over macroscopic distances. The soft matter systems investigated here demonstrate the possibility of molecularly engineering photoactuators that mimic functions we associate with living organisms. Bilayered or multilayered structures are widespread across a broad range of plant and animal tissues and their architectures contribute to their complex biological functions. For example, the anisotropic layers of cellulose fibrils in plants induce hygroscopic actuation in response to humidity and govern the opening and closing of pine cones,1Dawson C. Vincent J.F.V. Rocca A.M. How pine cones open.Nature. 1997; 390: 668Crossref Scopus (350) Google Scholar direct the pumping movements of wheat awns that propel seeds to the ground,2Elbaum R. Zaltzman L. Burgert I. Fratzl P. The role of wheat awns in the seed dispersal unit.Science. 2007; 316: 884-886Crossref PubMed Scopus (392) Google Scholar and trigger the reversible origami-like folding and unfolding of ice plant seedpods.3Harrington M.J. Razghandi K. Ditsch F. Guiducci L. Rueggeberg M. Dunlop J.W.C. Fratzl P. Neinhuis C. Burgert I. Origami-like unfolding of hydro-actuated ice plant seed capsules.Nat. Commun. 2011; 2: 337Crossref PubMed Scopus (169) Google Scholar Inspired by these natural systems, layered synthetic materials and devices across different length scales have been developed for mechanical actuation applications. By combining a layer of an actuating material with a “passive” non-actuating component, it is possible to achieve an anisotropic deformation rather than the isotropic expansion or contraction expected for the actuating component alone. This effect has been demonstrated using many different bilayered or multilayered materials with components such as solid polymer films,4Tada A. Geng Y.F. Wei Q.S. Hashimoto K. Tajima K. Tailoring organic heterojunction interfaces in bilayer polymer photovoltaic devices.Nat. Mater. 2011; 10: 450-455Crossref PubMed Scopus (248) Google Scholar, 5Kharlampieva E. Kozlovskaya V. Sukhishvili S.A. Layer-by-layer hydrogen-bonded polymer films: from fundamentals to applications.Adv. Mater. 2009; 21: 3053-3065Crossref Scopus (337) Google Scholar, 6Khan M.K. Hamad W.Y. MacLachlan M.J. Tunable mesoporous bilayer photonic resins with chiral nematic structures and actuator properties.Adv. Mater. 2014; 26: 2323-2328Crossref PubMed Scopus (74) Google Scholar, 7Wang S. Gao Y. Wei A. Xiao P. Liang Y. Lu W. Chen C., Zhang C., Yang G., Yao H., Chen TAsymmetric elastoplasticity of stacked graphene assembly actualizes programmable untethered soft robotics.Nat. Commun. 2020; 11: 4359Crossref PubMed Scopus (50) Google Scholar, 8Liu S. Yao Z. Chiou K. Stupp S.I. Olvera de la Cruz M. Emergent perversions in the buckling of heterogeneous elastic strips.Proc. Natl. Acad. Sci. USA. 2016; 113: 7100-7105Crossref PubMed Scopus (19) Google Scholar liquid crystal elastomers,9Boothby J.M. Ware T.H. Dual-responsive, shape-switching bilayers enabled by liquid crystal elastomers.Soft Matter. 2017; 13: 4349-4356Crossref PubMed Google Scholar,10Agrawal A. Yun T.H. Pesek S.L. Chapman W.G. Verduzco R. Shape-responsive liquid crystal elastomer bilayers.Soft Matter. 2014; 10: 1411-1415Crossref PubMed Google Scholar and hydrogels.11Le X. Lu W. Zhang J. Chen T. Recent progress in biomimetic anisotropic hydrogel actuators.Adv. Sci. 2019; 6: 1801584Crossref Scopus (176) Google Scholar, 12Liu G. Ding Z. Yuan Q. Xie H. Gu Z. Multi-layered hydrogels for biomedical applications.Front. Chem. 2018; 6: 439Crossref PubMed Scopus (19) Google Scholar, 13He X. Zhang D. Wu J. Wang Y. Chen F. Fan P. Zhong M., Xiao S., Yang JOne-pot and one-step fabrication of salt-responsive bilayer hydrogels with 2D and 3D shape transformations.Acs Appl. Mater. Interfaces. 2019; 11: 25417-25426Crossref PubMed Scopus (19) Google Scholar, 14Hu Z. Zhang X. Li Y. Synthesis and application of modulated polymer gels.Science. 1995; 269: 525-527Crossref PubMed Scopus (458) Google Scholar Hydrogels are unique soft matter for such actuation applications due to their hydrated nature and ability to change volume by absorbing or expelling water.15Ionov L. Hydrogel-based actuators: possibilities and limitations.Mater. Today. 2014; 17: 494-503Crossref Scopus (427) Google Scholar,16Erol O. Pantula A. Liu W. Gracias D.H. Transformer hydrogels: a review.Adv. Mater. Technol. 2019; 4: 1900043Crossref Scopus (121) Google Scholar Two particularly noteworthy examples include 4D-printed cellulose-based bilayer architectures that change shape upon immersion in water17Gladman A.S. Matsumoto E.A. Nuzzo R.G. Mahadevan L. Lewis J.A. Biomimetic 4D printing.Nat. Mater. 2016; 15: 413-418Crossref PubMed Scopus (1522) Google Scholar and gel structures photopatterned with multiple domains that allow localized actuation in response to DNA sequences complementary to those domains.18Cangialosi A. Yoon C. Liu J. Huang Q. Guo J. Nguyen T.D. Gracias D.H., Schulman RDNA sequence-directed shape change of photopatterned hydrogels via high-degree swelling.Science. 2017; 357: 1126-1129Crossref PubMed Scopus (203) Google Scholar Bilayer hydrogels have also been reported in which the two layers have components that are both stimuli responsive, leading to bending in one direction or the other depending on the stimulus.13He X. Zhang D. Wu J. Wang Y. Chen F. Fan P. Zhong M., Xiao S., Yang JOne-pot and one-step fabrication of salt-responsive bilayer hydrogels with 2D and 3D shape transformations.Acs Appl. Mater. Interfaces. 2019; 11: 25417-25426Crossref PubMed Scopus (19) Google Scholar,19Cheng Y. Ren K. Yang D. Wei J. Bilayer-type fluorescence hydrogels with intelligent response serve as temperature/pH driven soft actuators.Sensor Actuat. B-Chem. 2018; 255: 3117-3126Crossref Scopus (69) Google Scholar, 20Zhang Z.H. Chen Z. Wang Y. Chi J. Wang Y. Zhao Y. Bioinspired bilayer structural color hydrogel actuator with multienvironment responsiveness and survivability.Small Methods. 2019; 3: 1900519Crossref Scopus (34) Google Scholar, 21Li X. Cai X. Gao Y. Serpe M.J. Reversible bidirectional bending of hydrogel-based bilayer actuators.J. Mater. Chem. B. 2017; 5: 2804-2812Crossref PubMed Scopus (77) Google Scholar, 22Li J. Ma Q. Xu Y. Yang M. Wu Q. Wang F. Sun PHighly bidirectional bendable actuator engineered by LCST-UCST bilayer hydrogel with enhanced interface.ACS Appl. Mater. Interfaces. 2020; 12: 55290-55298Crossref PubMed Scopus (17) Google Scholar Light is a particularly useful stimulus since it does not require physical contact with materials and also because of the versatility offered by wavelength and intensity tunability.23Li Q. Schenning A.P.H.J. Bunning T.J. Light-responsive smart soft matter technologies.Adv. Opt. Mater. 2019; 7: 1901160Crossref Scopus (23) Google Scholar, 24Bertrand O. Gohy J.F. Photo-responsive polymers: synthesis and applications.Polym. Chem. 2017; 8: 52-73Crossref Google Scholar, 25Gelebart A.H. Mulder D.J. Varga M. Konya A. Vantomme G. Meijer E.W. Selinger R.L.B., Broer D.JMaking waves in a photoactive polymer film.Nature. 2017; 546: 632-636Crossref PubMed Scopus (464) Google Scholar, 26Hu Y. Li Z. Lan T. Chen W. Photoactuators for direct optical-to-mechanical energy conversion: from nanocomponent assembly to macroscopic deformation.Adv. Mater. 2016; 28: 10548-10556Crossref PubMed Scopus (90) Google Scholar, 27Ruskowitz E.R. DeForest C.A. Photoresponsive biomaterials for targeted drug delivery and 4D cell culture.Nat. Rev. Mater. 2018; 3: 17087Crossref Scopus (193) Google Scholar This versatility can be used in photoresponsive materials, such as liquid crystal networks (LCNs)28Cheng Y.C. Lu H.C. Lee X. Zeng H. Priimagi A. Kirigami-based light-induced shape-morphing and locomotion.Adv. Mater. 2020; 32: 1906233Crossref Scopus (59) Google Scholar and hydrogels,29Li L. Scheiger J.M. Levkin P.A. Design and applications of photoresponsive hydrogels.Adv. Mater. 2019; 31: 1807333Crossref Scopus (167) Google Scholar, 30Takashima Y. Hatanaka S. Otsubo M. Nakahata M. Kakuta T. Hashidzume A. Yamaguchi H., Harada AExpansion-contraction of photoresponsive artificial muscle regulated by host-guest interactions.Nat. Commun. 2012; 3: 1270Crossref PubMed Scopus (476) Google Scholar, 31Lee T.T. García J.R. Paez J.I. Singh A. Phelps E.A. Weis S. Shafiq Z., Shekaran A., del Campo A., García A.JLight-triggered in vivo activation of adhesive peptides regulates cell adhesion, inflammation and vascularization of biomaterials.Nat. Mater. 2015; 14: 352-360Crossref PubMed Scopus (300) Google Scholar, 32Ouyang L.L. Highley C.B. Sun W. Burdick J.A. A generalizable strategy for the 3D bioprinting of hydrogels from nonviscous photo-crosslinkable inks.Adv. Mater. 2017; 29: 1604983Crossref Scopus (269) Google Scholar functionalized with molecular photoswitches.33Russew M.M. Hecht S. Photoswitches: from molecules to materials.Adv. Mater. 2010; 22: 3348-3360Crossref PubMed Scopus (728) Google Scholar, 34Pianowski Z.L. Recent implementations of molecular photoswitches into smart materials and biological systems.Chem. Eur. J. 2019; 25: 5128-5144Crossref PubMed Scopus (129) Google Scholar, 35Mogaki R. Okuro K. Aida T. Adhesive photoswitch: selective photochemical modulation of enzymes under physiological conditions.J. Am. Chem. Soc. 2017; 139: 10072-10078Crossref PubMed Scopus (37) Google Scholar In these systems, conformational changes as a result of photoisomerization can lead to the macroscopic shape changes in hydrogels.36Chen J. Leung F.K.-C. Stuart M.C.A. Kajitani T. Fukushima T. van der Giessen E. Feringa B.LArtificial muscle-like function from hierarchical supramolecular assembly of photoresponsive molecular motors.Nat. Chem. 2018; 10: 132-138Crossref PubMed Scopus (191) Google Scholar, 37Li C. Iscen A. Sai H. Sato K. Sather N.A. Chin S.M. Álvarez Z., Palmer L.C., Schatz G.C., Stupp S.ISupramolecular-covalent hybrid polymers for light-activated mechanical actuation.Nat. Mater. 2020; 19: 900-909Crossref PubMed Scopus (61) Google Scholar, 38Foy J.T. Li Q. Goujon A. Colard-Itté J-R. Fuks G. Moulin E. Schiffmann O., Dattler D., Funeriu D.P., Giuseppone NDual-light control of nanomachines that integrate motor and modulator subunits.Nat. Nanotech. 2017; 12: 540-545Crossref PubMed Scopus (119) Google Scholar, 39Lancia F. Ryabchun A. Katsonis N. Life-like motion driven by artificial molecular machines.Nat. Rev. Chem. 2019; 3: 536-551Crossref Scopus (107) Google Scholar For example, photocontraction of hydrogels through the isomerization of protonated merocyanine (MCH+) to spiropyran (SP) moieties40Kortekaas L. Browne W.R. The evolution of spiropyran: fundamentals and progress of an extraordinarily versatile photochrome.Chem. Soc. Rev. 2019; 48: 3406-3424Crossref PubMed Google Scholar,41Klajn R. Spiropyran-based dynamic materials.Chem. Soc. Rev. 2014; 43: 148-184Crossref PubMed Google Scholar is a well-known phenomenon.42Sumaru K. Ohi K. Takagi T. Kanamori T. Shinbo T. Photoresponsive properties of poly(N-isopropylacrylamide) hydrogel partly modified with spirobenzopyran.Langmuir. 2006; 22: 4353-4356Crossref PubMed Scopus (131) Google Scholar, 43Francis W. Dunne A. Delaney C. Florea L. Diamond D. Spiropyran based hydrogels actuators—walking in the light.Sensor Actuat. B Chem. 2017; 250: 608-616Crossref Scopus (63) Google Scholar, 44Satoh T. Sumaru K. Takagi T. Kanamori T. Fast-reversible light-driven hydrogels consisting of spirobenzopyran-functionalized poly(N-isopropylacrylamide).Soft Matter. 2011; 7: 8030-8034Crossref Scopus (90) Google Scholar, 45Li C. Lau G.C. Yuan H. Aggarwal A. Dominguez V.L. Liu S. Sai H., Palmer L.C., Sather N.A., Pearson T.J., et alFast and programmable locomotion of hydrogel-metal hybrids under light and magnetic fields.Sci. Robot. 2020; 6: eabb9822Crossref Scopus (32) Google Scholar In recent work we reported on the synthesis of water-soluble spiropyran structures covalently embedded in a 3D hydrogel network that led to photoexpansion of hydrogels.46Li C. Iscen A. Palmer L.C. Schatz G.C. Stupp S.I. Light-driven expansion of spiropyran hydrogels.J. Am. Chem. Soc. 2020; 142: 8447-8453Crossref PubMed Scopus (60) Google Scholar Previously reported examples of deformation and actuation are based on photoisomerization gradients, but layered spiropyran-based materials have not been reported. Using a combination of both photocontracting and photoexpanding layers that are simultaneously responsive to a single light stimulus, we report here on the design of synergistic bilayer photoactuators and investigate their unique photoactuation behavior. Here, we prepared a series of bilayer structures in which individual layers expand, contract, or remain unresponsive to light. The photoexpanding layer is composed of a poly(N-isopropylacrylamide) (PNIPAM) backbone grafted with a water-soluble spiropyran moiety bearing two negatively charged sulfonate substituents (SP1). Photoisomerization of the protonated merocyanine (MCH−) to the spiropyran (SP2−) form caused an increase in net charge density, resulting in hydrogels that absorb water molecules thus expanding to 130% of their original dimension (Figure 1A). On the other hand, the photocontracting layer contains the same PNIPAM backbone with a different hydrophobic spiropyran moiety (SP2) that has a similar absorbance spectrum (Figure S1A) and a comparable photoisomerization rate (Figure S1B). The resulting photocontracting material displayed similar mechanical properties (Figure S2) to the photoexpanding layer. Upon irradiation with the same light, it isomerizes from the MCH+ to the SP form and the decrease in net charge density drives the hydrogel to expel water and contract to 83% of its initial volume (Figure 1B). Photoinactive layers without spiropyran moieties were used here as the light-unresponsive layers (Figure 1C). A two-step free radical polymerization procedure was used to glue each individual layer to obtain four different bilayer objects in total (each 10 mm long, 2 mm wide, and containing two 0.3 mm layers, see the Experimental procedures and Supplemental information for details), namely exp-con (expansion-contraction), exp-bl (expansion-blank), bl-con (blank-contraction), and bl-bl (blank-blank, bottom layer-top layer). We fabricated the bilayers by partially polymerizing the first layer followed by addition of the second set of precursors and initiating polymerization of the second layer to ensure chemical linking of the two layers, which is critical for their structural stability as actuators. Cross-sectional scanning electron microscopy of these bilayer samples revealed that they are tightly adhered to each other at their interface (Figure S3). Confocal laser scanning microscopy also confirmed the adhesion of the two bonded layers (Figure S4). These four bilayer objects were found to display different photoactuation behavior under the same light illumination because objects containing photoactive layers bend up, while the photoinactive bl-bl bilayer keeps its flat geometry (Figure 1D). Interestingly, the synergistic exp-con bilayer object showed a larger bending angle (78°) relative to either the exp-bl (48°) or bl-con (45°) bilayers (Figure 1E; Video S1), indicating that the combination of expanding and contracting layers generates a greater deformation gradient responsible for the observed shape changes. In addition, synergistic bilayer objects create a faster bending speed (13°/min) by a factor of ∼4–5 relative to that of either exp-bl (3°/min) or bl-con bilayers (2.8°/min). This acceleration was also observed during the relaxation process in the dark, when spiropyran moieties spontaneously switched back to the more thermally stable form of protonated merocyanine and the bending objects recovered to their original flat state. It was found that the relaxation time of synergistic exp-con bilayer was 15 min, whereas 20 min was required for relaxation of the exp-bl bilayers and 90 min for the bl-con bilayers. Video S2 shows the first 40 min of the recovery process of these three bilayers, but the bl-con bilayer actuator does not fully recover to its original flat shape within this period of time. The reason for the slow recovery of the bl-con bilayer might be that the contracting layer containing SP2 becomes denser upon irradiation, which in turn slows water diffusion and recovery to its initial shape under dark conditions. By switching light on and off, these bilayer objects were able to bend and unbend for multiple cycles (Figure S5), demonstrating the high reversibility and robustness of this actuation system. https://www.cell.com/cms/asset/82998751-3f8c-4dd3-8ccd-9873da666571/mmc2.mp4Loading ... Download .mp4 (4.74 MB) Help with .mp4 files Video S1. Light-activated bending behaviors of different bilayer objectsEach object is 10 mm long, 2 mm wide, and contains two 0.3 mm layers. https://www.cell.com/cms/asset/3eadbb4e-79ea-4897-ad94-d0e05971f3c9/mmc3.mp4Loading ... Download .mp4 (1.5 MB) Help with .mp4 files Video S2. Relaxation behaviors of different bilayer objects in the darkEach object is 10 mm long, 2 mm wide, and contains two 0.3 mm layers. In addition to PNIPAM, we also prepared synergistic bilayer photoactuators using polyacrylamide (PAM), which is not thermally responsive. The original dimensions of the photoexpanding (PAM-SP1) and photocontracting layers (PAM-SP2) changed to 116% and 87% of their original dimensions upon light irradiation, respectively (Figures S6A and S6B). These volumetric changes, especially the photoexpansion ratio, were found to be smaller than those observed in PNIPAM-SP hydrogels, which is consistent with our previous finding that spiropyran-containing polymer hydrogels with a higher lower critical solution temperature (LCST) exhibit a lower photoexpanding ratio.46Li C. Iscen A. Palmer L.C. Schatz G.C. Stupp S.I. Light-driven expansion of spiropyran hydrogels.J. Am. Chem. Soc. 2020; 142: 8447-8453Crossref PubMed Scopus (60) Google Scholar Because of the smaller volumetric change, the synergistic bilayer containing PAM was found to display a smaller bending angle and a slower bending rate compared with one containing PNIPAM under the same irradiation conditions (Figures S6C and S6D). These results offered us an additional strategy to tune the photoactuation performance of the synergistic bilayer actuators by simply changing polymer composition. The concept of synergistic bilayer photoactuation to enhance performance was also tested in hydrogel objects with different dimensions. Figure 2A shows that exp-con bilayer objects display larger bending angles with increasing aspect ratio (fixing thickness and width but increasing length) (Figure S7). This observation was in good agreement with the calculated results from the analytical model (linear dashed lines, see the Experimental procedures for details), which predicted the slope of this curve to be greater by a factor of ∼2.0 for exp-con bilayer objects relative to that for exp-bl and bl-con bilayers. We investigated how the thickness of each layer affects the overall deformation behavior while keeping the aspect ratio at a fixed value. For this purpose, we define η as the thickness ratio between the top and bottom layers. As shown in Figure 2B, the analytical model verified that the bending angle of a bilayer with synergistic behavior (exp-con) tends to be larger than that of either the exp-bl or bl-con bilayers, indicating that the synergy is valid over different thickness ratios of the two layers. More importantly, all three curves are nearly flat, suggesting that the bending angle should be nearly independent of the relative thicknesses of the two layers (η) over the range 0.5–2.0. The slight increase at low values and minimal decline at high values of η indicated that the bending angle tends to be optimal when η is close to 1. Therefore, in subsequent experiments we used bilayer objects with a fixed η value of 1.0 and a fixed thickness of 0.3 mm for each layer. To gain more insight into the driving force generated during photoactuation, we calculated the bending moment that is required to flatten the bent bilayer using our analytical model (see the Experimental procedures for details). Figure S8 shows that the model predicts the synergistic exp-con bilayer to have a nearly 2-fold greater bending moment (2.0 × 10−7 N‧m) relative to that of the exp-bl and bl-con bilayers. We suggest this difference explains the enhanced actuation performance observed in the synergistic bilayer system. Based on its actuation performance, the synergistic exp-con bilayer was used to further design functional structures that are capable of programmable shape changes in response to light. We prepared rectangular bilayer constructs as photoactive units and define exp-con (bottom layer-top layer) units as −1 and the inverted unit con-exp as 1 (Figure 3A). After assembling these photoactive units (1 or −1) into a desired predetermined sequence, a solution containing NIPAM monomers was added and polymerized to join these photoactive units. A series of linear structures with specific sequences of photoactive and photoinactive units were prepared and are listed in Figure 3B (see the Experimental procedures and Supplemental information for details). The linear structures (Lin-1 to Lin-8) contained a total of four photoactive units (i–iv) and maintained identical flat geometry in the dark (Figure S9). However, these flat objects exhibited clear 3D bending and folding behaviors upon irradiation with visible light (450 nm) (Figure 3C; Video S3). These photo-induced origami-like shape changes were programmed by predetermined permutations of the four photoactive units. This programmability allows us to create light-activated shape transformations, which are predicted with finite element simulations by fitting the experimental parameters, such as moduli and expansion/contraction strain (Figure 3C, bottom; see the Experimental procedures and Supplemental information for details). Following the same principle, we designed and prepared cross-shaped structures containing eight photoactive units with variable permutations of 1 and −1 that can transform into complex 3D geometries upon irradiation with visible light (Video S4). Figure 3D illustrates four different permutations as well as their corresponding 3D configurations from both experiments (top) and simulations (bottom). In addition, we designed a branched structure containing a total of 12 photoactive units that exhibited a more complex configuration upon irradiation with visible light (Figure 3E; Video S5). The abrupt shape changes observed in Videos S3, S4, and S5, are likely due to friction between the hydrogel actuator and the substrate. The hydrogel actuator requires a sufficient bending force to overcome the friction before an actual shape change can occur. This bending force originates from the light-induced gradient of expansion/contraction between the two layers, which is a slow process. If the bending force is smaller than the critical value needed to overcome the friction at a time point, then no shape change occurs. However, once the bending force exceeds this friction, the hydrogel object rapidly changes shape due to a rapid release of free energy. Importantly, all these shape transformations are highly reversible, as the bending structures gradually recover their original flat shapes in the dark due to spiropyran moieties switching back to the merocyanine structure. https://www.cell.com/cms/asset/e04321b0-893d-449b-8025-87c78026a08b/mmc4.mp4Loading ... Download .mp4 (4.08 MB) Help with .mp4 files Video S3. Light-activated origami-like shape changes of linear structuresEight linear structures with predetermined permutations of 1 (con-exp) and −1 (exp-con) are shown. https://www.cell.com/cms/asset/08858aa0-0488-4464-be25-296e40c518b9/mmc5.mp4Loading ... Download .mp4 (5.46 MB) Help with .mp4 files Video S4. Light-activated origami-like shape changes of cross-shaped structuresFour cross-shaped structures with predetermined permutations of 1 (con-exp) and −1 (exp-con) are shown. https://www.cell.com/cms/asset/01413452-5e19-44fd-998d-04b51a34b597/mmc6.mp4Loading ... Download .mp4 (9.32 MB) Help with .mp4 files Video S5. Light-activated origami-like shape changes of a branch structure with predetermined permutations of 1 (con-exp) and −1 (exp-con)Both front and side views are shown. To demonstrate potential robotic functions, such as locomotion of these shape-morphing objects, we built millimeter-scale ratcheted structures at the bottom of some of the photoinactive segments using a ratchet mold transfer method (see the Experimental procedures and Supplemental information for details). The hydrogel objects with these anisotropic ratchets exhibited anisotropic friction with the substrate they were in contact with during shape transformation, which in turn we found could be used to control their locomotion direction. Figure 4A illustrates two types of inchworm-like walkers (code (−1)11(−1) for walker 1 and (−1)1(−1)1(−1) for walker 2) whose front and back feet are functionalized with the ratchets. Due to anisotropic friction with the substrate, the front foot stands still while the back foot moves forward during the photo-induced bending process. Conversely, the front foot moves forward while the back foot stands still during the flattening process once the light is off. Consequently, the walkers move forward unidirectionally for one single step. By alternately switching the light on and off, multi-step unidirectional locomotion from left to right was achieved, in good agreement with the results from finite element simulations (Figure 4B; Video S6). The spacing between front and back feet changed alternately along with the light being switched on and off, and the centroid of the object moved forward smoothly over a macroscopic distance over four walking cycles (107 mm for walker 1; 120 mm for walker 2, Figure 4C), indicating the high reversibility and robustness of the systems. In contrast to previously reported actuators that can only walk on specific substrates containing special features, the direction of this inchworm-like motion is determined by the built-in rachets and does not rely on the features or roughness of the substrate. https://www.cell.com/cms/asset/b3554960-d790-4172-8ca8-f806dfdb33f8/mmc7.mp4Loading ... Download .mp4 (4.5 MB) Help with .mp4 files Video S6. Unidirectional inchworm-like walking motionFour walking cycles of walker (−1)11(−1) (top) and walker (−1)1(−1)1(−1) (bottom) after alternating periods of light on and off are shown. Finite element simulation results are shown right below the experimental results. To expand locomotion gait, we developed a cross-shaped hydrogel walker with four feet containing built-in ratcheted patterns and obtained motion similar to that of an octopus. The ratchets were aligned perpendicular to the walking axis to obtain better control of unidirectional movement. Figure 5A illustrates the walking mechanism based on the bending–flattening process by switching the light on and off. Unlike the inchworm-like movement discussed previously, the front feet collapsed in the direction perpendicular to the walking motion instead of completely standing still during the bending process under irradiation. Also, the back feet relaxed in the direction perpendicular to the walking motion while the front feet moved forward during the flattening process in the dark. Consequently, a unidirectional octopus-like motion was achieved, which could be repeated and cycled multiple times by switching the light on and off (Figure 5B) to achieve macroscopic locomotion (Figure 5C; Video S7). This octopus-like walking behavior was also investigated by finite element simulations (see the Experimental procedures for details). https://www.cell.com/cms/asset/968f3fdd-5202-412a-8a15-04a5e9f6a298/mmc8.mp4Loading ... Download .mp4 (5.25 MB) Help with .mp4 files Video S7. Unidirectional octopus-like walking motionFour walking cycles of a cross-shaped object after alternating periods of light on and off. Finite element simulation results are shown right below the experimental results. We have designed and synthesized photoactive bilayer hydrogel actuators that respond to a single stimulus of light through the synergistic effect of photoexpansion and photocontraction. The synergistic photoactuator displayed a larger deformation gradient between the two layers and a faster reversible bending/relaxing speed relative to conventional actuators in which only one layer is photoresponsive. Encoding these bilayers into linear, cross-shaped, and branched hydrogel structures with a predetermined sequence, enabled highly programmed shape transformations upon light irradiation. By incorporating anisotropic ratcheted patterns into their bodies, these hydrogel objects exhibited improved motions over macroscopic distances by alternately switching the light source on and off, and the walking motions were independent of the substrate features. Importantly, all these shape changes and the locomotion observed in experiments were predicted by finite element simulations. We anticipate that the biomimetic strategy to create synergistic bilayer photoactuators demonstrated here will benefit the design and development of other functional soft materials that mimic or surpass the functions observed in living organisms. Furthermore, the use of such bilayer hydrogels could enable their application as responsive biomaterials and could be designed to involve stimuli other than light.