Light-driven micron-scale 3D hydrogel actuator produced by two-photon polymerization microfabrication

Journal Pre-proof Light-driven micron-scale 3D hydrogel actuator produced by two-photon polymerization microfabrication Chenglin Zheng, Feng Jin, Yuanyuan Zhao, Meiling Zheng, Jie Liu, Xianzi Dong, Zhong Xiong, Yanzhi Xia, Xuanming Duan

PII:

S0925-4005(19)31544-8

DOI:

https://doi.org/10.1016/j.snb.2019.127345

Reference:

SNB 127345

To appear in:

Sensors and Actuators: B. Chemical

Received Date:

2 August 2019

Revised Date:

23 October 2019

Accepted Date:

25 October 2019

Please cite this article as: Zheng C, Jin F, Zhao Y, Zheng M, Liu J, Dong X, Xiong Z, Xia Y, Duan X, Light-driven micron-scale 3D hydrogel actuator produced by two-photon polymerization microfabrication, Sensors and Actuators: B. Chemical (2019), doi: https://doi.org/10.1016/j.snb.2019.127345

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[Title Page] Light-driven micron-scale 3D hydrogel actuator produced by two-photon polymerization microfabrication

Chenglin Zheng a,b,1, Feng Jin c,1, Yuanyuan Zhaod, Meiling Zhengc,⁎, Jie Liuc, Xianzi

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Dongc, Zhong Xionga,b,*, Yanzhi Xiab, Xuanming Duand,⁎.

College of Chemistry and Chemical Engineering, College of Materials Science and Engineering, Qingdao University, Qingdao 266071, P. R. China.

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Institute of Marine Biobased Materials, Shandong Collaborative Innovation Center of

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Marine Biobased Fibers and Ecological textiles, State Key Laboratory of Bio-fibers

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and Eco-textiles, Qingdao University, Qingdao 266071, P. R. China Laboratory of Organic NanoPhotonics and CAS Key Laboratory of Bio-Inspired

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Materials and Interfacial Science, Technical Institute of Physics and Chemistry, Chinese Academy of Sciences, No. 29, Zhongguancun East Road, Beijing, 100190, P.

d

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R. China.

Guangdong Provincial Key Laboratory of Optical Fiber Sensing and Communications,

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Institute of Photonics Technology, Jinan University, 855 East Xingye Avenue, Panyu

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District, Guangzhou, 511443, P. R. China.

*

Corresponding author. E-mail address: [email protected] (Z. Xiong), [email protected] (M. Zheng), [email protected] (X. Duan) 1 C. Zheng and F. Jin contributed equally to this work.

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Graphical abstract

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Highlights

Near-infrared-light-driven micron-scale 3D hydrogel actuators were successfully

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manufactured by TPP microfabrication.

A gel photoresist for TPP was developed and the actuators were composed of

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photothermal PNIPAM/nano-Fe3O4 hydrogel. The size of the double-armed hydrogel microactuator was only ~26 m and the

The actuation response showed good repeatability and controllability.

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light response time was ~0.033 s.

Abstract

Light-driven micro/nano-actuators are one of the most important topics in the biomedical micro-electromechanical systems (MEMS) field. Currently, their

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development is hampered due to the difficulties in designing and fabricating biocompatible light-driven microactuators with the dimensions less than one hundred micrometres and a response time in the order of seconds. In this work, gel photoresists were prepared by embedding photothermal surface-modified Fe3O4 nanoparticles (NPs) into a mixture that included a photoinitiator, photosensitizer, monomers, crosslinkers and solvents. Macroscopic poly(N-isopropylacrylamide) (PNIPAM)/nano-Fe3O4

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hydrogels were prepared by ultraviolet photopolymerization of gel photoresists, which showed good temperature-responsive volume changes and light-triggered bending

deformation. Then the two-photon polymerization (TPP) microfabrication properties of gel photoresists with 0, 0.48 and 0.95 wt% Fe3O4 NPs were investigated in detail.

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Importantly, after the TPP microfabrication and subsequent solvent-exchange procedure,

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a double-armed near-infrared (NIR)-light-driven three-dimensional (3D) hydrogel microcantilever with a size of ~26 m was successfully fabricated. The hydrogel

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microactuator had a fast response time of ~0.033 s in water under NIR radiation and showed good reversibility. Furthermore, the distance between the two arms of the

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hydrogel microcantilever could be manipulated by controlling the laser focus and

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incident laser power.

Keywords: 3D hydrogel microstructure; Actuator; Two-photon polymerization; Light-driven; Photoresist

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1. Introduction In the past ten years, micro/nano-actuators have become the main focus of research topics such as micro-electromechanical systems (MEMS) [1, 2], optoelectronics [3], robotic systems [4] and microfluidic systems [5]. One of the current trends of MEMS is miniaturisation and portability, which requires the incorporation of complex computing circuitry, power sources and electrically driven actuators into miniaturised systems [6,

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7]. Conventional microactuators are usually driven by pneumatic [8], electromagnetic [9] and piezoelectric [10] approaches, in which size reduction of the microdevices to less than 100 microns is very difficult. Light-driving is an attractive and green approach

because of the non-contact, rapid, precise and remote control of microactuators [11−13].

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Huang et al. [14] fabricated a swimming microrobot with a polymer gripper containing

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the azobenzene chromophore. By periodically flashing ultraviolet (UV) and white light, the microrobot flagellum swung to eventually push the robot forward in a liquid

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environment. The gripper on the robot head could be opened or closed in response to light to grab and carry a load. The dimension of the light-driven gripper surpassed 2 mm.

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Zhang and Sun’s group [15] reported centimetre sized light-driven floating devices with a superhydrophobic, photothermal active layer prepared through direct laser writing of

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polydimethylsiloxane (PDMS) elastomers. By integrating the functional layer at the desired position or by designing asymmetric structures, three light-driven devices (fish,

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dozer boat, and gear) with fast linear or rotational motions were obtained. Generally, there are three problems hindering the application of light-driven microactuators in the biomedical field [16−19]: i) large sizes of the manufactured actuators, up to hundreds of micrometres and even millimetres; ii) poor biocompatibility of the materials; iii) slow response to external light, with response times up to minutes. Accordingly, current

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challenges involve designing and fabricating biocompatible light-driven microactuators with dimensions less than one hundred micrometres and response times at the second level. Two-photon polymerization (TPP) is a powerful technology for three-dimensional (3D) micro/nano-fabrication that has gained popularity in MEMS and the biological field in the past decade [20−25]. Two-photon photopolymerization can be initiated by

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nonlinear absorption of tightly focused, femtosecond laser pulses, which leads to localized crosslinking of photosensitive materials within the focal volume, resulting in arbitrary 3D construction with high-precision [26, 27]. TPP microfabrication has been extensively applied to manufacture micro-optical components [28],

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micro/nano-machines [29, 30], tissue engineering devices [31, 32], etc. Interestingly,

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light-driven devices, such as microsprings [20], microrotors [33], microtweezers [34] and micropumps [35], have been fabricated through TPP since the early stages of the

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development of this technique. The dimension of the microdevices was about ~10 m, which could be manipulated using a laser tweezer technique. Unfortunately, most of the

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microdevices were constructed with commercial TPP photoresins, composed of acrylic or acrylate-based oligomers, which resulted in poor biocompatibility [26, 32].

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Hydrogels are defined as 3D polymer networks capable of absorbing water that can highly resemble the extracellular matrix and thus have excellent biocompatibility with

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living organisms. Therefore, they are widely used in tissue engineering and drug delivery [36, 37]. Hydrogels have the unique feature of undergoing significant volume changes in response to diverse external stimuli, such as pH, temperature, light, electric field, the presence of chemicals or any combination of them [38−41]. Generally, light-triggered actuation of hydrogels includes two types: photoisomerization/ionization

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of chromophores and photothermal heating of chromophores or nanoparticles in thermoresponsive matrices [42−45]. Hardy et al. [46] prepared a light-responsive hydrogel microneedle 425 m high and 315 m wide by micromolding. Due to the existence of a light-responsive ibuprofen conjugate, hydrogel-forming microneedle arrays enabled the delivery of a clinically relevant model drug (ibuprofen) upon UV light irradiation at 365 nm. In 2002, Watanabe et al. [47] first achieved the two-photon

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microfabrication of polymer hydrogels. They constructed a ~100 m 3D hydrogel microcantilever via TPP and observed a bending behaviour caused by localized swelling under UV light irradiation. Pennacchio et al. [48] developed a gelatin-based hydrogel that could be finely micropatterned by TPP and stimulated in a controlled manner by

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light irradiation thanks to the presence of an azobenzene crosslinker. Light-triggered

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expansion of gelatin microstructures induced an in-plane nuclear deformation of physically confined NIH-3T3 cells by 10 min laser radiation at 700 nm. To the best of

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our knowledge, up to now, the fabrication of light-driven 3D hydrogel microdevices of several tens of micrometres and response times in the order of seconds remains a

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challenge. In this paper, light-driven microactuators consisting of photothermal poly(N-isopropylacrylamide) (PNIPAM)/nano-Fe3O4 hydrogels were successfully

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obtained by TPP microfabrication. The micron-scale 3D hydrogel actuator, with a size

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of ~26 m, exhibits a fast light-response time.

2. Experimental section 2.1 Materials

Benzil as a photoinitiator and 2-benyl-2-(dimethylamino)-4′-morpholinobutyrophe-

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none as a photosensitizer were purchased from ACROS Organics and Shanghai TCI Development, respectively. N-Isopropylacrylamide (NIPAM) and poly(ethylene glycol) diacrylate (PEGDA, Mn ≈ 600) were acquired from Shanghai Aladdin Bio-Chem Technology. Acrylamide (AAM) was obtained from Shanghai Aibi Chemistry Preparation Co. Ltd. N, N'-Methylenebisacrylamide (MBA) was purchased from Chengdu Kelong Chemicals. 3-(Trimethoxysilyl)propyl methacrylate (MPS), which is a

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surface-modifier of the Fe3O4 NPs, was obtained from Qingdao Haihua Flameretardant Co. Ltd. All chemicals were of analytical grade and used without further purification.

2.2 Synthesis of photothermal surface-modified Fe3O4 NPs

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Scheme 1 displays the preparation procedure for the light-driven hydrogel

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microactuator. Fe3O4 NPs were synthesised via chemical co-precipitation according to our previous reports [49, 50]. For further grafting, Fe3O4 particles (4.6 g) were mixed

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with ethanol (300 mL) in a flask, then the surface-modifier MPS (3 g, 1.2 mmol) was added dropwise. The mixture was purged with nitrogen for 0.5 h at room temperature

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and then heated to reflux for 4 h with stirring under a nitrogen atmosphere. Afterwards, the obtained black powder was isolated using an NdFeB magnet, washed with ethanol

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three times to remove unreacted MPS absorbed on the particles, and dried under

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vacuum to yield MPS-Fe3O4 NPs.

2.3 Preparation of gel photoresist Typical preparation procedure of gel photoresist was as follows. As-synthesised

MPS-Fe3O4 NPs (0.018 g) were dispersed into a hydrophilic solvent consisting of ethanol (0.055 mL) and DMSO (0.264 mL), by ultrasonic oscillation. Then, the

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comonomers AAM (0.08 g) and NIPAM (0.4 g), crosslinkers PEGDA (0.2 g) and MBA (0.014 g), the photoinitiator benzil (26.2 mg) and photosensitizer 2-benyl-2-(dimethylamino)-4′-morpholinobutyrophenone (26.8 mg), and the thickener glycerol (0.8 g) were dissolved into the black mixture. The hybrid solution was allowed to stand for 1 h, resulting in a gel photoresist with 0.95 wt% Fe3O4 NPs. Three gel photoresists were prepared with different contents of MPS-Fe3O4 NPs: 0, 0.48, and 0.95

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wt%.

2.4 Preparation of light-driven hydrogel

The gel photoresist was photopolymerized in a sandwiched glass mould (length: 75.6

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mm, width: 25 mm, thickness: 0.2 mm) under the irradiation of a high voltage mercury

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lamp (power: 32.5 mW cm−2, wavelength: 365 nm) for 4 min. The resulting smooth gel was immersed in deionized water for 36 h at room temperature to remove the residual

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monomers, oligomers, and the hydrophilic solvents. Afterwards, the swelled hydrogel was cut into a rectangular strip (15.5 mm × 1.4 mm × 0.25 mm) with a V-notch in the

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middle (Fig. S1). Additionally, hydrogel discs were obtained by cutting gel samples

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with a hole punch (diameter: 8 mm) and then immersing in water.

2.5 TPP microfabrication

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A near-infrared (NIR) Ti: sapphire femtosecond laser beam (120 fs, 80 MHz, 780 nm)

was used to fabricate 3D hydrogel microstructures [50]. The laser beam was tightly focused using a 60× oil immersion objective lens with high numerical aperture (N.A. =1.42, Olympus). The focal point was set into the liquid gel photoresist, which was placed on a cover-glass slide above the xyz-step motorized stage of a piezoelectric

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nanopositioner (P-563.3 CL, Physik Instrument) controlled by a computer [50]. The glass substrate was cleaned and modified by immersing in MPS/toluene solution (5 wt%) overnight to increase the adhesion between the microstructures and glass surface. After microfabrication, the unpolymerized resin was sequentially washed with ethanol and deionized water. The sample on the glass slide was preserved in deionized water.

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2.6 Characterization The crystal structure of the MPS-Fe3O4 NPs was determined by X-ray diffraction

(XRD, DX2700, China) from 5 to 90° operating with Cu Kα radiation (λ =1.5418 Å) at a scan rate (2) of 2° min−1. The morphology, size, and lattice structure of the Fe3O4

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NPs were analysed using transmission electron microscopy (TEM, Tecnai G2 F20

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S-TWIN, FEI, USA) operated at an accelerating voltage of 200 kV. The chemical composition was investigated by X-ray photoelectron spectroscopy (XPS) using an

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ESCALab250Xi electron spectrometer (Thermo Fisher Scientific Corporation) with Al Kα radiation. Morphology observations and energy-dispersive spectroscopy (EDS)

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analysis of the microstructures were carried out by scanning electron microscopy (SEM, HITACHI S-4800). Infrared thermal imaging was achieved using a thermal imaging

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camera (Fotric288).

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3. Results and discussion 3.1 Design concept

In this paper, PNIPAM/nano-Fe3O4 nanocomposite hydrogel was selected as the

actuator material. These components were selected based on the following issues: (i) PNIPAM has been commonly used as a temperature-responsive hydrogel in many fields

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due to its ability to undergo a reversible lower critical solution temperature phase transition from a swollen, hydrated state to a shrunken, hydrophobic one [51]; (ii) black Fe3O4 NPs are a highly effective photothermal agent induced by NIR laser irradiation [52]. The photothermal effect allows heat to be rapidly generated under laser irradiation and heat can drive the PNIPAM hydrogel to shrink. Thus, by combining the PNIPAM and Fe3O4 NPs, the light-driven deformation of nanocomposite hydrogel can be

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achieved under NIR laser exposure. The phase transition or the swelling-shrinking of the hybrid hydrogel is completely reversible [45]. Although macroscopic

PNIPAM/nano-Fe3O4 hydrogels could be synthesised through a simple in situ

precipitation method [45], the TPP microfabrication of hydrogel microactuators

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remained a challenge because of the lack of efficient commercial water-soluble TPP

deposition of Fe3O4 NPs during TPP.

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initiators, polymerization instability due to the vast amount of solvent, and the

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The design of photoresists is based on the following considerations. First, since commercial water-soluble TPP initiators are rare and have low TPP initiating efficiency

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in aqueous solutions,24 oil-soluble photoinitiators and photosensitizers were utilized to prepare a gel photoresist containing hydrophilic organic solvents. A solvent-exchange

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strategy was used after TPP by immersing the gel in deionized water to exchange solvent molecules with water, which transforms an organic gel into a hydrogel.50

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Second, according to our previous studies,40,41 high viscosity raises the TPP stability and promotes polymerization, which can be explained by the “autoacceleration effect of free radical polymerizaiton” [53]. Therefore, viscous PEGDA was used as co-crosslinker and thickener, while glycerol was used as thickener and solvent. Third, the surface of Fe3O4 NPs was modified by MPS to improve the stability and dispersion

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of NPs in the gel photoresist. The fabrication route of the light-driven hydrogel microactuator (Scheme 1) comprised four steps: surface modification of co-precipitated Fe3O4 NPs, preparation of gel photoresist, TPP microfabrication of gel microactuators, and solvent exchange in water to induce the formation of light-driven hydrogel microstructures.

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3.2 Characterization of MPS-Fe3O4 NPs The wide angle XRD pattern of MPS-Fe3O4 NPs (Fig.1a) exhibits a series of

diffraction peaks in the 2 region of 5–90°. These can be assigned to the (111), (220), (311), (400), (422), (511), and (440) planes of a cubic inverse-spinel-structured Fe3O4

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(PDF card no. 65-3107) [54]. TEM image (Fig. 1b) shows that the mean size of the

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nanoparticles is around 7.7 nm, varying shapes from quasi-spheres to polyhedra. Fig. 1c shows a clear high resolution (HR)-TEM image of a single MPS-Fe3O4 particle, where

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detailed lattice fringes can be observed with a spacing of 0.297 nm, corresponding to the (220) plane of cubic Fe3O4. XPS was used to analyse the surface composition of the

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MPS-Fe3O4 NPs (Fig. 1d). The spectrum shows the presence of O 1s and Fe 2p; also, the peak at 284.4 eV was assigned to C 1s and the weak peak at 100.4 eV was related to

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of Si 2p, proving that the Fe3O4 NPs were grafted with MPS.

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3.3 Gel photoresist and thermally responsive hydrogel Fig. 2a shows the black gel photoresist containing 0.95 wt% MPS-Fe3O4 NPs, which

is very uniform. Even under gravitation, the NPs still formed a homogeneous and stable colloidal dispersion of the photopolymerizable resin for 12 h with no obvious solution stratification. Under UV light exposure for 4 min, the liquid gel photoresist polymerized

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into a disc-shape gel (Fig. 2a). UV-Vis transmission spectra of the gel photoresist with 0.95 wt% Fe3O4 NPs and without Fe3O4 NPs (samples diluted 20 times) are presented in Fig. 2b. For the photoresist without NPs, the transmittance of light was over 98.5% in the 500~850 nm region and the absorption was mainly observed at the UV light region (280~373 nm, black curve i of Fig. 2b), which was attributed to the photoinitiator and photosensitizer. After doping the gel photoresist with MPS-Fe3O4 NPs, the

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transmittance sharply declined in the 373~850 nm region (red curve ii of Fig. 2b). The maximal transmittance was under 33.3% within the 780~850 nm region, demonstrating that MPS-Fe3O4 NPs had good NIR absorption. It is worth mentioning that Fe3O4 NPs

were expected to absorb and transfer the light into thermal energy, instead the massive

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absorption by the organic compound and polymer network because the hydrogel

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polymer networks are actually more susceptible to damage by the focused laser. Accordingly, 660 and 780 nm radiation was used for the driving of macroscopic

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hydrogel strips and hydrogel microactuators, respectively.

The size changes of the nanocomposite hydrogel in response to temperature were

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measured. The photopolymerized gel disc (0.95 wt% Fe3O4) swelled from the original 8 mm diameter to 8.7 mm after immersion in water at 20 °C for 24 h (Fig. 2c). Through

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this procedure, unpolymerized monomers and oligomers were removed and the hydrophilic solvents inside the gel, including ethanol, DMSO and glycerol, were

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exchanged with water molecules, yielding a hybrid hydrogel. When increasing the water temperature to 80 °C, the hydrogel disc shrank 14.6%. Then, when decreasing the water temperature to 20 °C, the disc swelled and returned to its original state. These results demonstrated that the hydrogel has a reversible temperature response. The size change of the hydrogel samples at different temperatures is expressed by the deformation

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degree (D/D0), where D corresponds to the diameter of hydrogel at a specific temperature and D0 to the initial diameter of hydrogel at 20 °C in deionized water. The deformation degree of hydrogels with different contents of Fe3O4 NPs as a function of water temperature is summarised in Fig. 2d. Here, 0.95 wt% Fe3O4 content was used as the highest content in hydrogel and higher Fe3O4 content such as 1.45 and 2 wt% led to the instability of gel photoresist and unstable TPP. Obvious volume shrinking was

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observed for all the samples when the water temperature increased. The deformation degrees of the hydrogels at 80 °C were 0.802, 0.788, and 0.829 for 0, 0.48 and 0.95 wt% Fe3O4 content, respectively, indicating that the incorporation of Fe3O4 NPs had a very

small impact on the deformation. Moreover, the shrinking-swelling deformation of the

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hydrogel disc (Fe3O4 content: 0.95 wt%) could be repeated 20 times by alternating the

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water temperature between 20 and 80 °C, showing good reversibility (Fig. 2e).

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3.4 Light-driven deformation of hydrogel

Light-driven actuation was evaluated on a home-made system with a 660 nm laser

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(power: 90 mW, Fig. 3a). Hydrogel strips with a V-notch (Fig. S1) were immersed in water (~10 °C) and the deformation was recorded by a CCD monitor. The laser beam

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was focused at the middle of hydrogel strip, above the notch. Fig. 3b demonstrates that the hydrogel strip without Fe3O4 NPs had no response to incident light. Thermal

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infrared imaging of hydrogel strip showed that the highest temperature in the laser irradiated area was 11.3 °C. The strip with 0.48 wt% Fe3O4 NPs turned from an original bend state to a straight state with a (Supplementary Information Movie S1); the highest surface temperature reached 46.7 °C (Fig. 3c). The light-response time was ~1.28 s. When the irradiation stopped,

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the hydrogel returned to its initial bending state. The bending angle, maximum surface temperature and light-response time of the hydrogel strip with 0.95 wt% Fe3O4 NPs were ~19°, 51.8 °C, and ~0.668 s, respectively (Fig. 3d, Supplementary Information Movie S2). The response time is sharply shortened and the bending angle of ~19° is considered to be close to that of hydrogel strip with 0.48 wt% Fe3O4 NPs. From the deformation degree vs. temperature curves (Fig. 2d), thermal response volume

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deformation of hydrogel with 0.48 wt% Fe3O4 is larger than that with 0.95 wt% Fe3O4 from 10 °C to 80 °C, whereas the temperature of the latter (51.8 °C) under laser

irradiation is higher than that of the former (46.7 °C). The bending deformation is a

comprehensive result of temperature-responsive deformation and photothermal effect.

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These results prove that Fe3O4 NPs have a significant effect on the hydrogel

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deformation. On the one hand, suitable Fe3O4 content such as 0.48 wt% is beneficial for hydrogel deformation, and high Fe3O4 content such as 0.95 wt% reduces hydrogel

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deformation; on the other, high Fe3O4 content helps to enhance the photothermal conversion effect, raise the hydrogel temperature, and accelerate the response of the

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hybrid hydrogel.

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3.5 TPP microfabrication property

Laser threshold power and polymer line width are two key parameters to evaluate the

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processing accuracy of TPP microfabrication. The threshold energy is usually defined as the lowest average laser power which can produce solid polymer lines from a photoresist. To determine the laser threshold power and line width of the as-prepared gel photoresist, the relationship between the line width and the laser scanning power was investigated at a constant linear scanning speed of 6 m s−1 (Fig. 4). The TPP laser

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threshold powers of the photoresists with 0, 0.48, and 0.95 wt% Fe3O4 NPs were 3.2, 3.4, and 4.4 mW, respectively. The threshold energy increased with the increasing of Fe3O4 content, which is consistent with our previous report.50 This behaviour can be ascribed to the absorption of the 780 nm IR laser by the Fe3O4 NPs and the resulting decrease in laser energy for TPP. Processing below the laser threshold powers resulted in incomplete or cracked hydrogel lines (left of line 1 in Fig. 4b, d and f). As shown in

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Fig. 4a, the polymer line width narrowed as laser power decreased, which can be considered a general rule. However, at a laser scanning power of 3.6 mW, the line width dramatically decreased in the gel photoresist without Fe3O4 NPs. This may be explained by the existence of some weak stratification at the interface between the glass slide and

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gel photoresist, which would induce bilayer polymerization (Fig. 4c, lines 3 and 4).

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Interestingly, bilayer polymerization was not observed for the gel photoresists with 0.48 and 0.95 wt% Fe3O4 NPs. This demonstrates that MPS-modified Fe3O4 NPs improve

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the interface compatibility between the glass substrate and gel photoresist. The narrowest lines were 200, 311, and 433 nm for the gel photoresists with 0, 0.48, and

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0.95 wt% NPs, respectively. For the gel without NPs, the processed lines were straight and smooth; the incorporation of Fe3O4 NPs led to rough and twisted polymer lines

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(Fig.4d-g). Additionally, the NPs inside the gel photoresist increased TPP instability

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during processing.

3.6 Light-driven hydrogel microactuators A double-armed light-driven hydrogel microgripper was designed and fabricated

through TPP using the gel photoresist with 0.95 wt% Fe3O4 NPs (Fig. 5a and c). The length, width and height of the two microcantilevers were 24, 1.5 and 2 m,

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respectively. To shorten the fabricating time of 3D microstructure, laser scanning speed was raised to 110 m s−1, and the corresponding laser power was explored to be 11.1 mW to ensure a high integrity and accuracy. To ensure that the two microcantilevers deformed freely and produced a large light-driven deformation, two micropedestals (top: 8 m × 10 m × 6 m, bottom: 5 m × 10 m × 8 m, Scheme 1) were fabricated as a support where the microcantilevers were suspended. For the microfabrication of top and

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bottom micropedestal, the laser scanning speed was 110 m s−1, while the scanning power was 10.5 and 9.5 mW, respectively. Fig. 5a shows the SEM image of the dried

microstructure laying on the glass substrate, whose surface was rough. EDS analysis of

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a specific area of the top micropedestal, between the two microcantilevers, showed that

Fe, O, C, and Si were present (Fig. 5b), indicating that the Fe3O4 NPs were incorporated

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into the microstructure.

After microfabrication, the microstructure was developed with ethanol and then

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covered with water. The light-driven actuation was achieved using the same femtosecond laser with the wavelength of 780 nm and a power of 29.2 mW. In the

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light-driven response demonstration, the laser beam was focused on the surface of the top micropedestal between the two microcantilevers to induce volume shrinkage of the

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irradiated region of the micropedestal due to photothermal effect (Fig. 5c), which allowed the microcantilevers to close. Then, when the incident laser was turned off, the

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photothermal effect disappeared and the temperature of the micropedestal surface decreased, inducing the microcantilevers to return to their original state. We defined D as the distance between the tips of the two microcantilevers in a specific condition. In the original state, in water, the two microcantilever showed an opened shape with D1=6.5 m. When the laser was turned on, the microcantilevers closed with D1=3.6 m

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(Supplementary Information Movie S3). The change in distance (△D1) reached 2.9 m. It is worth mentioning that the “closing” deformation of the two microcantilevers was achieved with a response time of ~0.033 s. The light-response time is remarkably reduced compared with the hydrogel strip, which can be attributed to the size reduction of the microstructure. Under diffusion limited conditions, the equilibrium time, T, of a polymeric hydrogel can be calculated approximately by following formula [55].

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T∝L2/K Where L is the hydrogel dimension and K is the solvent diffusion constant in the

hydrogel. By reducing the size of the hydrogel structure, the response time can be

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shortened appreciably compared with bulk materials. As far as we know, it is the first time to shorten the light response times of hydrogel microdevices to tens of

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milliseconds order [56, 57]. When the laser irradiation was turned off, the two microcantilevers “opened” to return to its original shape quickly with a response time of

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~0.033 s. The actuation response showed good repeatability (Fig. 5d, images 3 and 4). Also, the deformation of the two microcantilevers could be adjusted by moving the laser

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focus. When the incident laser focus was moved down by 2 m along the Z axis (Fig. 5e), D2 was ~4.3 m and △D2 reduced to ~2 m at the closed state (Fig. 5f). Meanwhile,

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the light-response time of the “closing” deformation of the microactuator showed no

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obvious changes compared with that in Fig. 5d. The “open” and “close” actuation could be repeated 20 times with no obvious damages to the hydrogel microstructure (Fig. 5g, Supplementary Information Movie S4). Additionally, D could be adjusted by alternating the incident laser power, as shown in Fig. 5h. A high laser power induced a small D and the double-armed microactuator “closed” tightly. When the laser power surpassed 30 mW, the hydrogel microactuator began to scorch.

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4. Conclusions Micron-scale 3D NIR-light-driven hydrogel actuators with fast response were successfully fabricated through four steps: the synthesis of surface-modified Fe3O4 NPs, the preparation of a gel photoresist, TPP microfabrication and a solvent-exchange process. The light-triggered microactuators were composed of photothermal Fe3O4 NPs,

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with an average size of 7.7 nm, and thermally responsive crosslinked PNIPAM hydrogel. The size of the macroscopic nanocomposite hydrogel disc with 0.95 wt% Fe3O4 NPs reduced 14.6% when increasing the water temperature from 20 to 80 °C; the

shrinking-swelling deformation behaviour showed good reversibility. The hydrogel strip

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bent under irradiation with a 660 nm laser. The TPP characteristics of gel photoresists

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with 0, 0.48, and 0.95 wt% Fe3O4 NPs were investigated, and the corresponding shortest line widths were 200, 311, and 433 nm with a laser scanning speed of 6 m s−1,

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respectively. Finally, a double-armed light-driven hydrogel microactuator with a size of ~26 m was fabricated via TPP. To the best of our knowledge, the microactuator, which

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could ‘‘close’’ or ‘‘open’’ in response to light with a response time of ~0.033 s, is the fastest light-responsive hydrogel microdevice reported. The deformation response could

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be manipulated by moving the incident laser focus and alternating the laser power. Due to its biocompatibility, small dimension and fast response, the photoresponsive hydrogel

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microactuators could have numerous potential applications in the biomedical MEMS field. It is worth mentioning that Fe3O4 NPs can be magnetically actuated as well and the hydrogel devices are expected to be run using two modalities (light and magnetic field), which make them even more applicable. The further researches are underway.

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Declaration of interests

 The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

☒The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Acknowledgements This work was supported by the National Natural Science Foundation of China

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(61405100 and 51673208), the Natural Science Foundation of Shandong Province (ZR2012EMQ006), the National Key Research and Development Program of China

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(Grant No. 2016YFA0200501)

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Chenglin Zheng is a graduate student at Qingdao University. His main research topic is the fabrication of biomimetic polymer microstructures.

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Feng Jin is a senior engineer at the Technical Institute of Physics and Chemistry of Chinese Academy of Sciences. He received Ph.D. degree from the graduate school of Chinese Academy of Sciences. His research focuses on multi-photon polymerization of functional materials with optical, electronic and magnetic properties.

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Zhong Xiong received his Ph. D. degree from Technical Institute of Physics and Chemistry, Chinese Academy of Sciences in 2009. After that, he worked at College of Chemistry and Chemical Engineering, Qingdao University. He was promoted to an Associate Professor in 2017. His research interests focus on two-photon polymerization micro/nanofabrication of polymer hydrogel and superhydrophobic polymer surfaces.

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Figure Captions

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Scheme 1 Preparation of light-driven hydrogel microactuators.

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Fig.1 (a) XRD pattern, (b) TEM and (c) HRTEM images, and (d) XPS spectrum of the

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surface-modified Fe3O4 NPs.

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Fig.2 (a) Gel photoresist and UV-photopolymerized gel disc. (b) UV-Vis transmission

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spectra of the gel photoresist without Fe3O4 NPs (black curve i) and with 0.95 wt% Fe3O4 NPs (red curve ii). (c) Disc sample: after UV photopolymerization, in 20 °C

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water after solvent exchange, in 80 °C water, again in 20 °C water. (d) Deformation degree as a function of temperature for hydrogels with different contents of Fe3O4 NPs.

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(e) The deformation degree-temperature cycle curve for the nanocomposite hydrogel with 0.95 wt% Fe3O4 NPs.

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Fig.3 (a) Schematic of the experimental device for light-driven hydrogel strips. Light

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actuation behaviour of hydrogel strips with various contents of Fe3O4 NPs: (b) 0, (c)

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0.48 wt%, and (d) 0.95 wt%. (b), (c) and (d): 1. Image of hydrogel strip; 2. Vertical view of the strip fixed by a clamp; 3. Laser focused at the hydrogel; 4. Strip after laser

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is turned off; 5. Thermal infrared image of hydrogel strip under laser irradiation.

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Fig.4 (a) Line width vs. laser scanning power of gel photoresists with different contents of Fe3O4 NPs. SEM images of lines produced using photoresists with (b, c) 0, (d, e) 0.48

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wt%, and (f, g) 0.95 wt% of Fe3O4 NPs. The magnified images (c), (e) and (g) correspond to the selected areas in (b), (d) and (f). Scale bars are 2 m for (b), (d) and (f)

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and 500 nm for (c), (e) and (g).

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ro of -p re lP na ur Jo Fig.5 (a) SEM image of the hydrogel microactuator fabricated by TPP and (b) its corresponding EDS spectrum. (c) Scheme of NIR laser actuation. (d) Optical

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microscope photographs of the light-driven hydrogel microactuator. 1, 3: laser off; 2, 4: laser on. D is the distance between the two tips of the microcantilevers. (e) Scheme of light actuation when moving laser focus and (f) the corresponding hydrogel microactuator. (g) The D2-IR laser (on or off) cycling curve of the hydrogel microcantilever. (h) D3 vs. laser power in water for a hydrogel microcantilever. Scale

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bars: 10 m.

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