Chunyan Qin, Zhilian Yue, Nieves Casañ-Pastor, Jun Chen, Gordon Wallace. The promises and future directions of wireless stimulation in biomedical applications[J]. Materials Lab, 2023, 2(2): 220058. doi: 10.54227/mlab.20220058
Citation: Chunyan Qin, Zhilian Yue, Nieves Casañ-Pastor, Jun Chen, Gordon Wallace. The promises and future directions of wireless stimulation in biomedical applications[J]. Materials Lab, 2023, 2(2): 220058. doi: 10.54227/mlab.20220058

PERSPECTIVE

The promises and future directions of wireless stimulation in biomedical applications

More Information
  • Corresponding author: gwallace@uow.edu.au
  • Wireless stimulation (WS) technologies have been developed as powerful strategies to modulate cellular behaviour and biological activity remotely and noninvasively through wireless manipulation of electrical signal. These WS systems are constructed from the electrically stimulus-responsive materials (magnetoelectric, piezoelectric, optoelectronic, and bipolar electroactive materials) that are triggered by the primary driving force, general like magnetic field, ultrasound, light, and electric field. With a deeper understanding of the integral role of electrical stimulation played in biological cells, tissues, and organs, WS has become the promising technique to work on neural cell stimulation, for either functional or repair effects, and other biological activities including drug release, electroporation and cancer treatment. This paper summarises existing WS systems in accordance with the utilised stimulus-responsive materials. Also, future directions of WS in potential biomedical applications are discussed. Along with the development of emerging techniques such as bipolar electrochemistry and 3D printing, more effective WS systems will be allowed to apply in biosystems with a change of paradigm.


  • The rising notion of going wireless has been revolutionising and propelling conventional wired stimulation technologies forwards. To adapt different wireless stimulation (WS) systems for a wide range of applications in biology, various stimulus-responsive materials, such as magnetoelectric materials, piezoelectric materials, optoelectronic materials and bipolar electroactive materials have been developed.[14] These WS technologies have shown promising potential in remotely activating an isolated working electrode driven by external power sources.[57] Their operating processes are similar to those of wireless charging, in which the electric, magnetic or electromagnetic energy is converted to electrical currents through the use of an antenna in battery, inducing charge transfer processes in some cases. Thus, in WS systems, a primary driven force (e.g., magnetic field, ultrasonic, light and electric field) can be wirelessly delivered across cells, tissues and organs, and converted to a local electrical signal using stimulus-responsive materials to modulate the cellular behaviors.[14]

    In this Perspective, recent progress of WS in biomedical applications is summarised according to the classification of abovementioned stimulus-response type materials. Magnetoelectric, piezoelectric and optoelectronic materials based traditional WS systems (Table 1) are firstly introduced. Subsequently, electroactive conducting materials such as conjugated polymers or oxides used as implanted bipolar electrodes recently are also present. Notably, the future directions of WS systems in biomedical applications could be extended to point-of-care sensors, wearable bandages, and implantable patches with the development of materials modification. We focus mainly here on the WS system induced by bipolar electrochemistry technology, discussing the developing bioactive ink formulations and fabricating 3D bipolar bioactive structures using 3D printing.

    Table 1.  Summary of traditional WS systems based on the use of materials.
    Materials based WS systemsMagnetoelectric materialsPiezoelectric materialsOptoelectronic materials
    Mechanismsmagnetic field is converted to a local electric fieldmechanical stress is converted to a local electric fieldlight is converted to a local
    electric field
    Advantagesdeeper delivery without magnetic field undiminishedenhanced spatial localization and depth targetinggreater tissue penetration depth and
    spatial resolution
    Disadvantagesintrinsically weak coupling in materials affects effective stimulation; toxic and biostable issuestoxic and biostable issueslimited applications because of specific wavelengths; toxic and biostable issues
    Biomedical fieldscellular regulationneural stimulationcellular modulation
    References[1, 8-10][2, 11-18][3, 19-30]
     | Show Table
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    Magnetic field passing through tissue undiminished and without producing harmful effects endows its use in the wireless deeper delivery of electric stimuli to modulate neural activity.[8] In contrast to methods that rely on mechanical forces or electromagnetic induction, magnetoelectric materials have been created to convert an externally applied magnetic field to a localized electric field.[9] However, due to the weak coupling in intrinsically magnetoelectric materials, current studies focus on magnetoelectric composites, which combine a material in which strain and magnetization are coupled (magnetostriction) with a material in which strain and electrical polarization are coupled (piezoelectricity). Notably, Guduru et al. had incorporated cobalt ferrite (CoFe2O4) as the magnetostrictive component and barium titanate (BaTiO3) as the piezoelectric component to synthesize a 30 nm magnetoelectric core-shell composite.[1] By the use of this magnetoelectric composite nanoparticle, neural stimulation under a low-energy magnetic field with frequencies ranging from 0 to 20 Hz and amplitudes of 10 mT, as well as neural recording through electroencephalography (EEG) signals modulating, were both achieved at the same time. However, due of the lead in the piezoelectric component, which raises toxicity issues for deployment in biological environments, future research is sort of confined to that component. This brings out the necessity of evaluating the interface’s biostability, spatiotemporal selectivity and accuracy, and electrophysiological evidence of cellular regulation both in vitro and in vivo.[10]

    To date, vast quantities of research have been conducted that used ultrasound (US) to stimulate excitable cells and alter cognitive behaviour wirelessly in the central and peripheral nervous systems.[11,12] Low-intensity US can be deeply delivered to nervous tissue, resulting in transient modulation of neural activity, which has been utilised for clinical and home healthcare settings.[13] While when US as a longitudinal wave with a frequency that is higher than 20 Hz, it can cause a nanoparticle to vibrate along the transmission path and exert mechanical stress on it. Thus, use of piezoelectric nanomaterials, US has been applied as a primary driven force to convert mechanical stress to a local electric field via mechanoelectrical transduction. Early efforts have been invested into disperse the piezoelectric Zinc oxide nanowires, boron nitride nanotubes (BNNTs), barium titanate nanoparticles (BTNPs), gum Arabic-coated barium titanate nanoparticles into culture medium with PC 12, SH-SY5Y, and C2C12 cells.[2,14,15] When cells ingested the piezoelectric materials and stay in conjunction with US, current is produced for cell stimulation, promoting neurite outgrowth and increasing the spiking activity of neuronal networks. Piezoelectric polymers like polyvinylidene fluoride trifluoroethylene p(VDF-TrFE) film and electrospun p(VDF-TrFE) microfibers have been reported to improve the neurogenesis of PC 12 cells and guide neurite extension while employing synergetic US treatment in recent studies.[16] In addition, blending piezoelectric BTNPs into piezoelectric p(VDF-TrFE) film coupled with US have been explored in neural stimulation and modulation.[17,18] Therefore, US has shown to be an appealing, safe, non-invasive stimulation method with enhanced spatial localization and depth targeting in neuromodulation field compared with alternative methods.

    Light becomes a prospective modality for stimulating neuronal cells/tissues to control and treat various diseases and disorders due to its wide wavelengths for greater tissue penetration depth and spatial resolution.[19,20] Quantum dots (QDs) can convert light to an electric dipole (electron-hole pair) via quantum confinement once excitated, and the excitation wavelengths of QDs range from ultraviolet (UV) via visible to near-infrared (NIR). In the very early study, the NG108-15 cells could be depolarised and stimulated upon irradiation with 532 nm laser pulses when cultured on HgTe QDs/poly(dimethyldiallylammonium chloride).[21] This proved that a QDs-assisted optical-to-electrical cellular modulation was possible. Following that, huge amount of optical stimulation work have been investigate based on various substrates such as QDs, metals, inorganic and organic semiconductors to modulate cellular behavior utilising light.[2225] It is worth noting the organic conjugated polymers (OCP) are of particular interest since they combine highly tunable photoactive properties with easy fabrication and biocompatible with a variety of cell lines.[26,27] Typically, a fabricated device that integrated organic photovoltaic (OPV) active layer with organic bioelectronic interface (OBEI) to convert photons for electrical stimulation and neuron differentiation.[3,2830] Poly(3-hexylthiophene) (P3HT), P3HT:phenyl-C61-butyric acid methyl ester (PCBM) polymer-fullerene blends (P3HT:PCBM), P3HT:PCBM with Al/Ti coating or polypyrrole (PPy) are all very attractive photo-responsive active layers. PC 12 cells were seeded on the OPV/OBEI devices and exposed to white or NIR light. The cells were wirelessly stimulated during culturing, resulting in variable cell polarity and morphology.

    Compared to the conventional electrochemistry, bipolar electrochemistry (BPE) has continuously attracted public attention because of its outstanding features including the wireless manner of physical connection, the gradient potential distribution on the bipolar electrode in some geometries, the intense external electric field in electrolyte for triggering polarisation, low concentration of electrolyte requirement, possible electrophoresis process for charged species migration, and easy multiplexing because of no limitation in the number of the bipolar electrodes put at the same time, and the absence of limitation in shape and size of the bipolar electrode.[34] Recent interest has been ignited primarily for wireless neural cell stimulation driven by the BPE because it removes the need for a physical wire-electrical connection to the bipolar electrode by using an electric field to induce a controlled potential for driving electrochemical reactions.[35,36] Significantly, only recently, the effect of bipolar electrochemistry has been described in electrostimulation.[4,31,37]

    A work in 2018 has described a series of assays using biocompatible conducting metals (Au, Pt), electroactive oxides (IrOx and IrOx-TiO2 composites) and conducting polymers (PEDOT-PSS and polypyrrole grown in different conditions), where electrostimulation is performed for xenopus neural cell growth, and compared them with insulating material (glass). Neural growth was evidently enhanced in presence of bipolar electrodes and resulted different depending in the material.[37] A different prototype using polypyrrole (PPy) films with different dopants acting as 2D bipolar electrodes was developed by some authors of this work group (Fig. 1).[4,33] The dopants tested involve p-toluene sulfonic acid (pTS, a popular low molecular weight dopant), dextran sulfate (DS, a bioinert biopolymer dopant) and collagen type I (a major extracellular matrix protein). We have revealed reversible and reproducible bipolar electrochemical activity of PPy films in biological solutions such as phosphate-buffered saline (PBS) and cell culture medium. Notably this is achieved with a much lower driving voltage (≤ 1.0 V cm−1) compared to metallic bipolar electrodes,[38,39] and much lower than previous work using insulating materials (less than 50 mV mm−1 vs 150 mV mm−1). All the IrOx, PEDOT and PPy films undergo electrochemical doping with gradient colours across the surfaces, which has been supported by in situ spectroscopy. It has been assumed, because of the color changes, that a gradient doping occurs at the electroactive material, something that has been proven recently on IrOx by EDX and XAS spectroscopy, when the electrolyte contains Na+ ions.[40] The induced gradient doping can be controlled by changing the polarity of the voltage (+/-) applied to the driving electrodes, within the solvent potential window, but is specific of each material. Furthermore, a safe and robust methodology has been established for wireless neural cell stimulation and verified for significantly promoting neurite outgrowth with a DC voltage of 0.33 V cm-1 stimulation. The stimulated rat pheochromocytoma PC 12 cells showed enhanced proliferation and neurite outgrowth and branching when they were cultured on PPy-DS/collagen as a bipolar electrode.

    Fig. 1  Bipolar electroactive conjugated polymers based WS systems. Bipolar electrochemical activity of PPy was realised and enhanced with PMAS incorporation in biological solution, displaying gradient colours across the surfaces (left). Soft PPy matrix was obtained with removal of rigid substrate (middle). Both rat pheochromocytoma cell (PC 12) and human neuroblastoma cell (SH-SY5Y) differentiation was promoted due to the enhanced bipolar electroactivity and the addition of softness property (right).[4,3133] Copyright 2020, 2022 Elsevier Ltd.

    Here, CP films were primarily coated on rigid electronically conducting substrate such as fluorine doped tin oxide coated glass slide (FTO) [4,35] or Pt coated glass.[51] Glass possesses an interface with less desirable mechanical properties for interaction with living cells. To tackle this challenge, we have introduced poly(2-methoxyaniline-5-sulfonic acid) (PMAS) to enhance the electroactivity and poly(3,4-ethylenedioxythiophene)-poly(styrenesulfonate) (PEDOT-PSS) to provide physical and mechanical support.[31,32] PMAS is a redox active polyelectrolyte, and has been incorporated into PPy to improve a material with superior conductivity and with multiple redox centres.[41,42] This PPy-PMAS material has been demonstrated in supporting nerve and muscle cell proliferation and differentiation effectively using traditionally wired stimulation systems by our group.[43,44] More recently we have found PPy-PMAS material presents significant bipolar electrochemical properties.[31] Furthermore, with PEDOT-PSS acting as a mechanical support while retaining softness and pliability in the overall structure, the prepared PPy-PMAS-collagen/PEDOT-PSS films were soft, free-standing and large size. Notably, the enhanced bipolar electrochemical performance and cytocompatibility, results in a significant increase in PC 12 cell number and neurite formation/growth. We have also evaluated human cell behaviour using SH- SY5Y cells, which demonstrated greater cell differentiation and neuron expression. Therefore, combining this BPE with conducting electroactive materials within biological media provides an exciting new dimension to wireless bioelectronics and electroceuticals.

    As discussed above, the WS systems using the stimulus-responsive materials have been largely developed in cell and tissue engineering field. In particular, the electroactive materials in bipolar configuration have demonstrated to functionalise and stimulate neural cells with the use of bipolar electrochemical reactions in wireless electroceuticals. Taking the wireless nature, the BPE also could be applied in sensor fields for electroanalysis in biological microfluidics.[45] Since bipolar electrode focusing for ions enrichment/locomotion has been revealed by Crooks and co-workers, lots of researchers focus on using the synergetic effects of electrophoresis and electrolysis in wireless electrofluidics for detection/separation of complicated biological fluid samples.[4648] Thus, except bioanalytical detection, WS systems would be further applied in practical applications like wearable bandages for fast healing, implantable patches for regeneration and restoration as long as the developed materials are with high-performance, biocompatible and biostable.

    WS systems have been widely well-established in neuroscience and clinical therapies. For example, the deep brain stimulation (DBS) technology has been broadly utilised for treating chronic pain and mental disorders such as Alzheimer disease with manipulating electrical stimulation of targets.[49,50] When the medical device is implanted in the human body, the surrounding environment immediately responds to the material itself. Thus, the softness of material is highly desirable because it could reduce tissue trauma during implantation. Also, the material must be biocompatible during all stages and should not cause immune and inflammatory reactions, although all foreign bodies do to some extent. The goal of in vitro live/dead or development test is to provide initial assessment of the cytotoxicity of the material on surrounding cells. If the material is not well matched with the cells, it is hard for the implanted devices to remain in place long term and it could result in unknown side-effects on the host. Therefore, the biocompatibility and long-term biostability of materials have been ongoing challenges during the development of WS systems in biomedical applications. In the following paragraphs, we focus on introducing how to improve the properties of bipolar electroactive materials using material compositions modification with additional engineering of the material structures design. We hope it will help maximize the efficacy of WS systems, making them provide well-controlled, therapeutically relevant effects.

    CP compositions containing an appropriate combination of extracellular matrix (ECM) protein and growth factor could be developed as bipolar electrode materials. ECM proteins including collagen I, fibronectin, laminin and aminoacid, have been identified as a co-dopant to produce PPy-PMAS-collagen, PPy-PMAS-fibronectin and PPy-PMAS-laminin respectively, working on cell growth and differentiation,[4,31,33,51] and also PPy-aminoacid and PEDOT-aminoacid.[52] In addition to ECM proteins, sustained neurotrophic support in close proximity to the electrodes is essential to maintain intimate interaction between the electrodes and cells.[53,54] We have previously shown in 2D hard-wired CP systems that the incorporation of growth factors such as neurotrophins (NT3) and brain-derived neurotrophic factor (BDNF) can further amplify the effects of electrical stimulation, using spiral ganglion neuron explants from rat cochleae.[55,56] Therefore, the lead CP compositions established in the above studies will be further modified by inclusion of BDNF and/or NT-3.

    The lead bioactive CP composition above established and PEDOT-PSS particles will be mixed in an aqueous solution containing diethylene glycol to form a uniform dispersion. The composition and total solid content of the CP ink will be screened in terms of rheological behaviour and printability. CP films will be prepared using these formulations and the respective mechanical and BPE activities will be determined. A 3D lattice pattern (Fig. 2a) will be selected for use in optimisation of basic printing conditions including temperature, extrusion rate, flow rate and nozzle diameter (50-200 μm). The 3D printed structures will be dried and annealed at 37oC. We will examine the effects of various printing parameters on the 3D printed structures. Fig. 2a-b also illustrates other 3D patterns that will be explored in the future. Depending on the targeted structures, a commercial GeSim BioScaffold Printer or a custom-designed 3D extrusion printer developed by the Translation Research Initiative of Cellular Engineering and Printing (TRICEP) at the University of Wollongong will be employed for 3D Printing. Where necessary, we will explore innovative printing methods such as coaxial printing and hybrid printing as described by us previously.[57,58]

    Fig. 2  Schematic of various 3D printed bipolar electroactive architectures. a Lattice and cylindrical structures and b nerve conduits.

    Bioactive bioink formulations using the above CP compositions and 3D bipolar structures using 3D printing would be developed to further promote the WS in biomedical applications. For example, cells could be introduced into selected 3D printed structure with and without encapsulation in the hydrogels to support cytocompatibility and neurogenesis study. A 3D WS protocol in selected 3D printed structures could be developed because BPE works without need of wiring to a power supply. The effects of hydrogel inclusion on the BPE activities of the 3D integrated structures are worthy to be investigated in the presence or absence of cells.

    Therefore, to further promote the WS systems in neuroscience and clinical therapies, various material modification methods should be explored to improve the biocompatibility and long-term biostability of materials themselves in the future work. In the meantime, the development of emerging techniques such as BPE and 3D printing also allows more effective WS systems in biosystems with new vision. We believe the combination of material modification methods and emerging techniques will help maximize the efficacy of WS systems, making them provide well-controlled, therapeutically relevant effects.

  • This work was financially supported by the funding from the Australian Research Council (ARC) (CE140100012 and DP230101369) and Australian National Fabrication Facility (ANFF) - Materials Node at University of Wollongong (UOW), and Spanish AEI grants PID2021-123276OB-I00, and CEX2019-000917-S.

  • The authors declare no conflict of interest.

  • C. Qin, J. Chen conceptualized the idea. C. Qin wrote original draft. J. Chen, N. CP has participated in discussions, developed the original ideas and acquired and handle funding. G. G. Wallace administrated project and acquired funding. All authors had reviewed, edited, and approved the final version.

  • Chunyan Qin is currently a postdoctoral research fellow at Intelligent Polymer Research Institute (IPRI), University of Wollongong (UOW). She received her PhD degree there in 2022. Her research interests lie in biomaterials, bio interfaces, cell culture/stimulation, drug delivery, biosensors, biomedical devices etc. In 2019, she received the Bill Wheeler Award for best communicating the social impact of her bionics research.
    ZhilianYue is currently a principle research fellow in the intelligent Polymer Research Institute, University of Wollongong. Her research interests include tissue engineering and regenerative medicine, 3D bioprinting and medical bionics.
    Nieves Casañ-Pastor is Research Professor at teh CSIC Institut de Ciencia de Materials de Barcelona, Spain. Her reserach interests are electroactive materials with mixed valence and mixed conductivity as electrodes, and the local resolution required to characterize gradient materials, as well as the implications in biostimulation and energy storage. She has been CSIC Scientific Comitte a¡Advisor and has recieved a number of Grants and Awards.
    Jun Chen is currently appointed as Associate Dean of Australian Institute for Innovative Materials (AIIM), and Head of Postgraduate Studies of IPRI/UOW. His research interests include electroactive materials, catalysis, sustainable energy devices/systems, electro-/bio-interfaces, nano/micro- materials, 2D/3D printing and wearable electronic devices. He has authored over 260 peer-reviewed publications in international journals with an h-index of 78. Chen has been identified as Highly Cited Researchers in Cross Field (2018|2020-2022) and received Vice-Chancellor's Award for Researcher of the Year (UOW) in 2021.
    Gordon G. Wallace is director of IPRI, ACES, and ANFF (Materials Node). He leads a world-class integrated multidisciplinary and multi-organisational team with a global impact in the design and utilisation of electromaterials for bionics. His research has resulted in excess of 1,020 refereed publications, with more than 50,000 citations, and an h-index of 103. The quality of CI Wallace’s work is attested by the June 2018 data from the Clarivate Analytics’ Essential Science Indicators lists, which rank the top 1% of authors of papers and 1% of papers by citations, published in the last 10 years.
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  • Table 1.  Summary of traditional WS systems based on the use of materials.
    Materials based WS systemsMagnetoelectric materialsPiezoelectric materialsOptoelectronic materials
    Mechanismsmagnetic field is converted to a local electric fieldmechanical stress is converted to a local electric fieldlight is converted to a local
    electric field
    Advantagesdeeper delivery without magnetic field undiminishedenhanced spatial localization and depth targetinggreater tissue penetration depth and
    spatial resolution
    Disadvantagesintrinsically weak coupling in materials affects effective stimulation; toxic and biostable issuestoxic and biostable issueslimited applications because of specific wavelengths; toxic and biostable issues
    Biomedical fieldscellular regulationneural stimulationcellular modulation
    References[1, 8-10][2, 11-18][3, 19-30]
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