Bio-Inspired Soft Robotics: Tunable Photo-Actuation Behavior of Azo Chromophore Containing Liquid Crystalline Elastomers

Featured Application

Inspired by nature, mechanical and material engineers construct innovative operating robotic models. Bio-inspiration always sparks novel ideas to design smart materials and structures for the development of innovative robots.

Abstract

Bio-inspiration relentlessly sparks the novel ideas to develop innovative soft robotic structures from smart materials. The conceptual soft robotic designs inspired by biomimetic routes have resulted in pioneering research contributions based on the understanding of the material selection and actuation properties. In an attempt to overcome the hazardous injuries, soft robotic systems are used subsequently to ensure safe human–robot interaction. In contrast to dielectric elastomer actuators, prolific efforts were made by understanding the photo-actuating properties of liquid crystalline elastomers (LCEs) containing azo-derivatives to construct mechanical structures and tiny portable robots for specific technological applications. The structure and material properties of these stimuli-responsive polymers can skillfully be controlled by light. In this short technical note, we highlight the potential high-tech importance and the photo-actuation behavior of some remarkable LCEs with azobenzene chromophores.

1. Introduction

Liquid crystalline elastomers (LCEs) are a new unique class of material derived from the combination of elasticity properties (like in an elastomer) and orientational order of mesogenic building blocks (liquid crystalline molecular array). Typically, mesogenic units are incorporated as flexible spacers to build linear polymer liquid crystal macromolecules [1,2,3]. Since the monodomain alignment of mesogenic groups was thermodynamically unstable, due to its spontaneous conversion into polydomain structures, researchers were only synthesizing polydomain side-chain LCEs until the pioneering research works of Küpfer and Finkelmann [4,5]. They introduced new two-step crosslinking conditions to develop monodomain LCEs, where initially a weak crosslinked network was constructed; later, this developed director orientation was replicated by the second crosslinking step via mechanical stretching to induce monodomain [6,7]. Evidently, for LCEs due to the coupling behavior of liquid crystalline order and the polymer backbone, external mechanical stress can considerably influence the state of an order [8,9]. The crosslinking process in different liquid crystalline phases (nematic or isotropic phase) highly influences the oriental distribution and results in different properties [10]. When the crosslinking was done in the nematic phase, the state of order was fixed within the crosslinking zones, leading to ‘frozen-in’ order. This can be achieved by exposing the sample to the applied mechanical stress perpendicular to the original direction of the monodomain [11,12,13]. The synthetic strategy proposed by Küpfer and Finkelmann for the preparation of monodomain nematic LCEs was sketched in Figure 1 with chemical structures used.

Over the last two decades, the booming progress in designing different types of LCEs with a variety of liquid crystalline phase has been noticed for the fine-tuning of the properties. Researchers investigated a wide variety of LCEs with diverse liquid crystalline phases including nematic, cholesteric (or helical), smectic phases (smectic A, smectic C, and smectic C *), and discotic and blue phases [14,15,16,17]. These LCEs with diversified liquid crystalline phases have been recognized as potentially effective to more technology-related topics, such as adaptive varifocal micro lenses in miniature electronic devices to soft actuator components of artificial muscle along with biomedical and soft robotic applications [18,19,20,21,22].

Some of the prominently studied polymers are outlined in Figure 2. The structure presented in Figure 2a comprise polyimides with azobenzene chromophores in the main chain and it was initially reported by Blair et al. [23]. Upon exposure to UV light, at the air/water interface, the stress diminution signpost the contraction of the monolayer. Under the dark condition, the stress increases again resulting in slight expansion of the monolayer. The photomechanical effects are caused by trans–cis photoisomerization of azobenzene chromophores (are more linear in their trans form than cis form) that can occupy a large surface area at the interface [23]. The polypeptide monolayers comprising two α-helical poly(γ-methyl L-glutamate) structures connected to azobenzene group prepared by Higuchi et al. [24] demonstrate the geometrical structural discrepancy during trans–cis photoisomerization resulting in the bending of the main chain (See Figure 2b). Menzel et al. [25] further investigated these photoresponsive behavior associated with polypeptides. The authors modified the structure (See Figure 2c) and introduced alky spacers. These monolayers demonstrated an expansion in UV light and contraction to the visible light. Upon exposure to UV light, the trans–cis photoisomerization created a huge increase in the dipole moment resulting in high affinity to the water surface [25]. The similar properties were observed by poly(vinyl alcohol)s enclosing azobenzene side chains (for structure, see Figure 2d) developed by Seki et al. [26].

In an effort to examine the structure–property relationships, a variety of symmetrical and unsymmetrical molecules was designed [27,28,29,30,31,32,33,34]. The bent-core (banana shape) mesogenic molecules with azobenzene chromophores are of special interest due to their structure relationships with light-triggered phase transition and photo-actuation properties [35,36,37,38]. These azobenzene, bent-core banana molecules were widely studied as intelligent stimuli-responsive materials for technological applications [39,40,41,42,43]. Merging the elastic property of polymeric elastomers and self-organizing properties of liquid crystals, many scientists have reported prospective works on crosslinked liquid crystalline polymers (CLCPs), which exhibit unique macroscopic shape-changing properties such as bending, contraction, and swirling especially under the influence of light. Most importantly, the photochemical phase transition of azobenzene chromophore (azotolane) containing CLCPs has a great influence on the photo-actuation (See Figure 3a–c.) [44,45,46,47,48,49,50]. In addition to azotolane moieties in the CLCP film, authors used other components such as platinum(II) tetraphenyltetrabenzoporphyrin (sensitizer) and 9,10-bis(diphenylphosphoryl)anthracene (annihilator) in order to trigger the trans-cis photoisomerization with 635-nm laser at a low power density of 200 mW cm⁻². The actuation performance was driven by low-power excited triplet−triplet annihilation based upconversion luminescence [50].

In brief, photoisomerization is a phenomenon of structural transformation of molecules under photo-excitation. Photoisomerization of azobenzene molecules was demonstrated in Figure 2d. The trans form (up) can be converted to the cis form (down) using ultra-violet (UV) radiation of wavelength of 300–400 nm. The visible light illumination of cis azobenzene at >400 nm can revert the molecule back to trans form. By applying heat to cis form, the molecule can also be relaxed to stable trans form. The photoisomerization process of azobenzene mesogens in CLCPs can result in induced molecular reorientation, and this is the source for photo-actuation [50,51,52,53,54]. The chemical structures of azobenzene chromophores (monomer and crosslinker) used to prepare photo-actuating liquid-crystalline gels (LCGs) by Ikeda et al. are shown in Figure 4 [51].

Yun et al. [52] studied azobenzene-doped liquid-crystal polymer (azo-LCP) prepared by “host-guest” method of fabrication process. 1,4-bis-[4-(3-acryloyloxypropyloxy)benzoyloxy]-2-methylbenzene was used as host and 4-4′-bis[6-(acryoloxy)hexyloxy]-azobenzene as guest material. The authors proposed that the azobenzene monomers elicit the alignment of the mesogens in two ways: (i) photoisomerization of azobenzene and rotation of azobenzene by means of a trans-cis-trans reorientation (TCTR), the latter was activated at around 365 nm. The authors evidently confirmed that the photo-bending speed of azo-LCP in the TCTR case is always faster than that of photo-isomerization (See Figure 5 for Sketch and bending snapshots of azo-LCP). The materials made of azo-LCP can precisely control the actuation that can advantageously be utilized in photo-driven soft robotics. The contraction of LCP along the major alignment direction of mesogens was favored by transformation of nematic to the isotropic phase of mesogens. Conversely, the shape of LCP is recovered when the mesogens transform from isotropic to the nematic phase. This can be achieved by visible-light irradiation [52].

Since many scientific efforts have been put forward to improve the photo-mechanical effect, the research works carried out by Garcia-Amorós et al. [53,54] interestingly studied the effect of different lengths of photo-active crosslinker spacer (4,4’-dialkoxyazobenzenes) on opto-mechanics of light-controlled actuators. The authors also proposed the incorporation of 4-alkoxy-4’-cyanoazobenzene chromophores as side chain monomers to nematic LCEs and obtained characteristic kinetic parameters for the thermal isomerization of this cyano-substituted azo chromophore and the final photo-actuator behavior was explained in detail [54]. The recent passionate growth in soft robotic designs offers new opportunities to construct simpler structures using soft polymeric materials like LCEs and dielectric elastomers. These can be utilized depending on the design objectivity and mechano-compatibility in soft robotics. The diversified approaches show that these stimuli-responsive soft materials have several applicational advantages in the development of artificial muscle-like actuators. Because of the combination of orientational order of liquid crystals and the elasticity of conventional rubbers, these materials can easily implementable in a wide range of technological fields from micromechanical systems to soft robotic haptic interfaces [55,56,57,58,59,60].

2. Light-Induced Response of Azobenzene Chromophores

On exposure to suitable wavelength of light, azobenzene chromophores show rapid response behavior. Due to this characteristic feature, azobenzene derivatives are widely used as photosensitive materials for a broad range of technological applications. In brief, two benzene rings link together with azo (-N = N-) functional group to form azobenzene chromophore. Functionalization of benzene ring can be done to prepare a variety of azobenzene derivatives by tuning electron-donating and withdrawing properties to achieve push–pull type azobenzene structures [61].

The fine-tuning of rigidity and flexibility of azobenzene molecules indorsed to unveil liquid crystalline (LC) behavior, which makes them extremely useful in designing photoresponsive materials. Under photo-excitation, the two isomeric configurations of azobenzene (a thermally stable trans state and a meta-stable cis form) undergo conversion from trans to cis state. During conversion, the molecule undergoes systematic geometrical deformation, which will end up with different molecular sizes for trans and cis forms (As shown in Figure 3d, the distance between reference carbon atoms of aromatic rings decrease from 9.0 Å to 5.5 Å, as the molecules transform from trans to cis state) [62].

One of the important parameters to consider in technical applications of a polymer is glass transition temperature (T_g). For a quick glance, T_g is a characteristic property of polymer and is related to the temperature where the molecular chains begin to move. The polymers containing azobenzene moieties can have switchable T_g and can induce reversible cis–trans photoisomerization. This photoswitching of T_g is a topic of scientific curiosity and technical importance. The first report involving T_g of azobenzene-containing polymers reported by Zhou et al. [63] proposed light-induced reversible solid-to-liquid transitions of the polymers. This strategy can be applied to heal the cracks in high-T_g polymers without harmful plasticizers. The authors also demonstrated that light can switch the T_g of the polymer, which eventually controls the mechanical properties of the polymers [63]. The polymers with switchable T_g developed by Zhou et al. are displayed in Figure 6. Since the ultraviolet (UV) irradiation of trans polymer powder samples not generated adequate amount of cis form, authors dissolved the trans polymer in dichloromethane (CH₂Cl₂) and stirred it under the illumination of UV light to achieve respective cis form. The authors also prepared two control samples to prove the liquefaction was not due to the residual solvents.

The differential scanning calorimetry (DSC) studies demonstrated that trans form showed a T_g of 48.0 °C and in both the heating curves (first and second), we can notice the two-phase transitions at 94.0 and 108.0 °C. However, for cis form, we can observe the T_g at −10.0 °C with broad exothermic peak at around 94.0 °C. Consequently, the study revealed that T_g of the polymer decreased with the cis content, serving as plasticizer [63].

Considerable attention has been focused on phase transition compounds especially where solid-to-liquid phase change involved. Under the influence of light, the molecular interaction in the solid state weakens to form a liquid state. This “photomelting” behavior of certain materials is of special interest in the material science field for the development of photosensitive materials. Despite diverse functional photomelting compounds are available, fast responsive materials are having superior significance to design bio-inspired robotic structures [64,65]. Based on photoswitchable T_g and “photomelting” behavior of azobenzene monomer, Yue et al. studied light-induced mechanical response in CLCPs. The photoresponsive moiety used by the authors is meta-methylazobenzene (M-azo), it was covalently crosslinked with dodecyl glyceryl itaconate (DGI) to construct CLCP films. The trans-to-cis photoisomerization of azo groups that CLCP network results in a photoswitchable T_g and performs reversible photomechanical motions upon exposure to UV/visible light [47]. As shown in Figure 6, the solid M-azo compound changes to liquid state. To trigger the transition, the solid M-azo compound was irradiated with UV light of wavelength 365 nm at an intensity of 125 mW cm⁻² for just 6 s. As the T_g of the polymer is closely associated with the mechanical properties of the polymers, the high T_g and storage modulus (140 MPa) was obtained for DGI/M-azo films before UV treatment. The lower Young’s modulus of 65.6 MPa was noticed in DGI/M-azo films after UV irradiation. This is due to the creation of cis-form in polymer films, which will reduce the T_g of the polymer. This photoswitchable T_g is exceptionally to achieve conspicuous photomechanical actuations of DGI/M-azo films under UV illumination. The authors evidently confirmed that bending and restoration of the films to original position were successfully controlled. This color-changing behavior of the films from orange to yellow was easily recognized (See Figure 7, Section: Photomechanical response of the CLCP film). This photoabsorption process is time-dependent. The irradiated light intensity plays a crucial role in deciding the degree of change in the T_g as well as response speed. By applying different intensity of irradiated light (3.28 to 45 mW cm⁻²), authors can control the bending speed of the film (0.4 to 2 mm s⁻¹) at ambient temperature [47].

As discoursed earlier (in Figure 1), based on the properties of siloxane CLCPs [5,66] and acrylic CLCPs, listed (in Figure 7) azobenzene chromophore containing LC materials will be utilized to fabricate CLCP films from one-step or two-step protocols. The fabricated CLCP films find their major application in the construction of photo-driven micro/macroactuators. Some of the prominent azobenzene-containing liquid crystalline (LC) materials (monomers and crosslinkers) utilized to prepare LCPs with polysiloxane and polyacrylate backbone are shown in Figure 8.

Braun et al. [72] studied the effect of azo crosslinkers on photo-actuation abilities of LCE systems in comparison to non-azo crosslinkers. For the construction of the LCE system, authors utilized varying quantities of azo crosslinkers, non-azo crosslinkers, and azo monomer (For chemical structures, see Figure 9). Since the phase transition of mesogens involved in the construction of LCE system is influenced by variation of applied temperature, the temperature dependency on the photo-actuation of LCE systems was studied. It was reported that an extraordinary robust photo-actuation of up to 34% was achieved using azo-crosslinkers at 70 °C. However weak photo-actuation (change in length) compared to thermal actuation was achieved using non-azo-crosslinkers. Irrespective of azo moieties, higher crosslinking agents are necessary to provide mechanical stability to the LCE systems, which eventually utilized in the mechanical actuation device applications. The mesogenic orientation during photo-actuation also influences the performance of the constructed devices. Therefore, the contribution of azo moieties in monomers and crosslinkers plays a pivotal role in deciding the photo-actuation performances of LCEs. The well-known photoresponsive azo-crosslinker (crystalline 74 °C nematic 91 °C isotropic) used in the work (Figure 9a) mostly performs the dimensional variations to produce bending actuation. The knowledge of optimizing the azo-crosslinkers in LCE films is also important to decide the stiffness and crosslinking structures, which ultimately decide the actuation performances of the LCE system. The authors denoted that even 100 µm thickness LCE film was uniaxially actuated without just bending actuation, perceiving strong photoresponse of 40% under white light (440 nm) illumination [72].

3. Bio-Inspired Application Prospects

The principle of biomimetics strives us to learn how nature has refined and not necessarily to imitate but redefine the characteristic qualities of natural systems that will be pertinent to designed robotic structures. One such possible way to explore the potential of biological principles present in nature is through their wide application in soft robotics. Currently, we can notice copious research works experiencing the design history approach for the re-examination of nature designs using technological tools. The most recent incarnation of synthetic efforts has been the development of functionally diverse LCPs in order to address customized applications in soft robotics [56,62,73,74,75,76,77]. To accomplish the basic mechanical winding and unwinding motions inspired by plant tendrils, Iamsaard et al. [78] developed the LCPs with azo-crosslinkers. A small quantity of chiral dopants (S-811) fine-tunes the liquid-crystal director to achieve a complex range of dynamic mechanical behavior that mimics plant tendril structures (see Figure 10 for chemical structures of chiral dopants used by Iamsaard et al. in addition to azobenzene monomers/crosslinkers for the preparation of CLCP films, which mimic the plant tendril structures. See Figure 11a for the photograph of a cucumber plant tendril with bending and chiral twisting distortions).

Inspired by the flapping motions of insect wings generating three-dimensional (3-D) motions like bending and twisting for the capability of agile flight, Lee et al. [79] synthesized azobenzene-based uniaxially aligned “monodomain” azo-liquid crystalline network [(azo-LCN) - designated here as MD-20CL)]. The developed LC polymer comparatively contains appropriate concentration (~20 wt. %) of azobenzene crosslinker to LC monomer used (Similar chemical structure, as shown in Figure 9a, but with six flexible -CH₂- spacers on both sides). The oscillatory responses were obtained after exposing MD-20CL cantilevers to 1.0 W cm⁻² of 442 nm. The authors evidently confirm that the dimensionality of the oscillations is strongly influenced by the alignment of nematic director to the cantilever. On exposure to coherent wave laser (442 nm), bending of the sample arise due to the development of non-uniform strain through the sample thickness. Whereas the modifications in the orientation of the nematic director generate a shear gradient that motives the twisting behavior of the cantilever. These flexural torsional oscillations replicate 3-D motions like bending, sweeping, and twisting to generate flapping motions [80]. The authors performed photopolymerization to achieve glassy, high modulus azo-LCN. Because of preferential alignment LC mesogens along the rubbing direction, the modulus of MD-20CL turns into anisotropic. The measured storage modulus measured parallel to nematic director was approximately 1 GPa and 0.6 GPa when measured perpendicular to nematic director [79].

The technical benefit of LCE material developed by Wang et al. [80] is advantageous because of the preparation of comparatively thick films despite LC alignment procedure, which is eventually useful in transmitting heavier loads. Taking the advantage of two-step crosslinking mechanism proposed by Küpfer and Finkelmann, two different pre-crosslinked LCE samples could be impulsively attached together during the second hydrosilylation crosslinking step, without using additional glues. As shown in Figure 11b,c, the LCE ribbons attain helical configurations in 8 s after exposing to near-infrared light source. The ribbons fully recover to their original shapes immediately after removing the light source. The authors concluded that the polysiloxane-based LCE system exhibits an astonishing pro in building multilayer hierarchical structures, which mimic a distinct plant tendril, which can also perform bending and chiral twisting (left-handed and right-handed) operations. Herein, the authors performed near-infrared light (center wavelength: 808 ± 3 nm, output power: 8 W) twisting actuation of the bilayer LCE ribbons. The change in the temperature caused by the heating effect of near-infrared light was prudently recorded using a thermal imager (FLUKE Ti90) to examine the curling behavior of LCE ribbons [76,80].

Mimicking underwater soft-bodied sea invertebrate’s locomotor movements is challenging. Precisely controlled deformations and physicomechanical properties of developed light-driven liquid crystal gels (LCGs) by Shahsavan et al. [81] promisingly control unhindered dynamic shape deformations and having substantial applications in technologies such as soft robots. The authors demonstrated different modes of underwater locomotion, by remotely actuating LCGs. Figure 12A schematically demonstrates the swimming mechanism of Hexabranchus sanguineus (Spanish dancer) based on a large-scale bending undulation along its central trunk. Figure 12B illustrates the schematic hybrid molecular alignment summarizing undulating flexion of the trunk in sea slugs. Figure 12C represents the chemical structure of mesogenic monomers and the photothermal agent used to prepare LCGs by Shahsavan et al. [81]. From thermal actuation investigations and finite-element simulations, the authors predicted huge and fast photothermal actuation of LCG samples in aqua media at ambient conditions (23 °C). the underwater bending of LCGs was performed by illuminating a 532-nm laser beam with different input powers. It was observed that the photothermal response of LCG-70 is almost 30 times higher than its pristine form. The studies revealed that the mechanical relaxation times in oscillatory mode is around 0.2 s [81].

As depicted in Figure 13a,b, Xiong et al. constructed soft photo-actuators based on LCPs driven by sunlight. The authors prepared agarose polymer films with homogeneously dispersed F-azo-1 compound. The films were equipped with piezoelectric transducer is polyvinylidene difluoride (PVDF) at the edge as shown in Figure 13b. When the film was exposed to sunlight, the instantly generated bending movement of the films was transferred to the PVDF generator, resulting in an open-circuit alternating voltage signal. An alternating voltage signal of 0.164 V was generated by this solar actuator (F-azo@AG) for continuous sunlight illumination of 6 s [82]. It was noted that many researchers are actively involved in visible-light responsive azopolymers considering damaging effects of UV radiation. For photo-actuators, various mechanical motions such as twirling, bending, contraction, rotation, twisting, and other motions for photo-actuators can be triggered by exposing to light. The most commonly observed phototropic plant; sunflower (Helianthus annuus) is the best example, which effectually responds to sunlight with mechanical motion [74,75,83]. Concerning the extendable durability, recently fluorinated azobenzene molecules [ortho-Fluoroazobenzene-(F-azo)] are synthesized and their remarkable stability was reported [84,85,86]. Excluding ultraviolet light stimulated photoisomerization, these F-azo compounds tune their transition from trans to cis form in visible wavelengths. Kumar et al. designed LC soft actuators with appropriate doping of F-azo-2 (Figure 13c) in addition to LC monomers and crosslinkers. The constructed films demonstrated their ability to self-propelling oscillatory motion upon sunlight exposure, as shown in Figure 13d [87].

Designing light-responsive soft actuators is quite challenging because the selection of materials for device applications involves the understanding of the inherent properties of chosen material. Many factors are to be considered for suitable importunities, such as response time, reversibility, cyclic stability, elastic modulus, etc., of used materials. In addition to LC materials, shape-memory materials (SMMs) and polymer gels plays a significant role in designing light-driven actuators made of soft elastic materials [88]. In order to improve the response time of gel-type actuators driven by light, Tamesue et al. [89] and Takashima et al. [90] reported curdlan polymer gels with host–guest interactions (such as a linear high molecular-weight β-1,3-glucan, decorated with α-cyclodextrins (α-CDs) as hosts and a poly(acrylic acid) with azobenzene pendants as guests). The works reported by Harada and coworkers involve the design strategy of covalently crosslinked poly-acrylamides decorated with both host α-CDs and azobenzene moieties [91]. These novel supramolecular gel materials are significant in performing reversible photo-deformation for many successful cycles and with fast response time (<1 s) Consequently, these supramolecular gel-actuators are fascinating and systems thereof suitable for artificial robots that can promisingly perform biomimicking sensitive gesticulations. Apart from azobenzene chromophores, some modified cyanine dyes and coordination complexes thereof can also have light absorption properties [92]. These dye-doped LCE systems can tune the material properties by synergic chemical bond interaction. In the future, the LCE systems with azobenzene monomers/crosslinkers with modified cyanine dyes and supramolecular gel materials decorated with azobenzene pendants can exhibit pronounced light absorption and photothermal properties, which can be useful in building soft robotic structures to perform biomimetic movements.

4. Conclusions

In this short report, we have discussed the latest developments involving azobenzene chromophores based LCEs. There is a consensus view emerging that these azobenzene chromophores incorporated LC elastomeric scaffolds can be distinctively utilized for potential applications in robotic wireless actuators and sensors. Covalent linkages and alignment of azobenzene chromophore mesogens play a pivotal role in the dynamic actuation behavior of elastomers under the influence of light [62]. The tunable photomechanical response of CLCP films under a precise wavelength of light can provide a promising opportunity to develop programmable LCP actuators for robotic tactile sensations [77]. Bio-inspiration striving exciting development of light-responsive LCPs by mimicking dynamic 3D motions existing in nature creation. It seems that certainly there are still many interesting design approaches that are awaiting to develop azobenzene mesogens, and involving them in various supramolecular/macromolecular assemblies, which can dynamically tune its mechanical response triggered by broad wavelength range [93].