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Nitrogen-Doped Graphene Combined With Bioactive Conducting Polymer: An Ideal Platform for Neural Interface.

INTRODUCTION

Neuroprosthetic electrodes are designed to facilitate functional restoration of a neural path related to disorders and traumas of the central nervous system (CNS), such as Parkinson's disease, retinitis pigmentosa, epilepsy, depression, and chronic pain [1-4]. The interaction between neural electrodes and neural tissues are via electrode interface, which can get targeted stimulation or recording. Simple metal electrodes used in active implantable devices suffer from fatal disadvantages of poor long -term stimulation and recording performance due to multiple intrinsic incompatibilities of the electrode materials with CNS [5, 6]. Studies indicate that the performance of electrode-tissue interface ultimately rests on the quality of the material substrate, which enables a long-lasting functional neural device [7, 8], In recent decades, great efforts have been made to modify the electrode surface with various materials that meet the requirements of creating an ideal interlayer between the external electrodes and neural tissue. In the physiological environment, bioelectric potentials are carried in electrolyte media in the form of ionic current and the purpose of the neural electrode is to transduce these bioelectric signals into electrical signals [9], Conducting polymers can pass electronic as well as ionic charges thanks to their molecular structure and have become promising candidate materials for the modification of electrode surface [10, 11]. Monomers based on heterocyclic aromatics, such as 3,4-ethylenedioxythiophene (EDOT) and pyrrole, have been widely investigated in this field [12-14],

Nanoscale components at neural interface are crucial factors for high-quality neural devices and the nexus of neurons and nanoscale materials can be traced from a large number of literatures [1, 15-17], To promote intimate neural tissue-electrode contact, which greatly improves the sensitivity of electrical communication at the interface, it is desirable to create new materials at nanoscale to "exchange" signals with extracellular matrix components. The large class of currently available nanomaterials contains those in carbon family, which have attracted great attention due to their inherent, remarkable electric conductivity and transport properties [18-20], It has been demonstrated that graphene coatings improve in vivo neural recording in American cockroaches and in vitro electrical stimulation [21], Most recently, nitrogen-doped graphene (g-[C.sub.3][N.sub.4]), two-dimensional (2D) graphitic-phase nanosheets, has been studied extensively in diverse fields such as supercapacitors, electrogenerated chemiluminescence, photocatalysis, and biological applications [22-25] due to its many superior properties such as low cost, nontoxicity, and ease of preparation [26]. g-[C.sub.3][N.sub.4] is composed of stacked layers and can be synthesized by facile thermolysis from cost-affordable precursors such as cyanamide, melamine, etc. [27, 28],

In this study, for the first time, we attempted to create a new composite material composed of g-[C.sub.3][N.sub.4] and PEDOT and apply it to neural electrode coating. Compared with polypyrrole, PEDOT was selected in our study because the ethylenedioxy bridge anchoring at the 3- and 4-positions of the thiophene ring results in a monomer with a lower band-gap and oxidation potentials, conferring the as-prepared polymer better long-term electrochemical stability. The nanocomposite of g-[C.sub.3][N.sub.4]/PEDOT possesses low impedance, high charge storage capacity (CSC), and excellent long-term stability compared with graphene/ PEDOT. Moreover, low cytotoxicity and good biocompatibility of g-[C.sub.3][N.sub.4]/PEDOT demonstrated by 3-(4,5-dimethylthiazol-2yl)-2,5-diphenyltetrazolium bromide (MTT) assay and in vitro cell culture ensure its safety when used as an interfacial material to contact neural tissue. The developed nanocomposite can be applied to the surface modification of neural electrodes thanks to its improved electrical performance, long-term electrochemical stability, and biocompatibility.

EXPERIMENTAL

Materials

Melamine, EDOT monomer, poly(styrene sulfate) (PSS), and NaCl were supplied by D & B Corporation, Ltd. (Shanghai, China). Graphene was purchased from Advanced Material Supplier Inc. (Nanjing, China). Glutaraldehyde (25% in [H.sub.2]O), osmium tetroxide (Os[O.sub.4], 4 wt% in [H.sub.2]O) and hexamethyl disilylamine (HMDS) were purchased from Aladdin (Shanghai, China). Phosphate buffered saline (PBS, pH 7.4) was purchased from Sangon (Shanghai, China). The reagents used in cell culture, including Dulbecco's modified Eagle's medium (DMEM), fetal bovine serum, horse serum, l-glutamine, streptomycin, and penicillin, were purchased from Nanjing Tengchun Biotechnology Development Co., Ltd (Nanjing, China). MTT, dimethyl sulfoxide (DMSO), goat serum, and antibodies were supplied by Sigma-Aldrich. Beef extract, peptone, and agar were purchased from Sinopharm Chemical Reagent Co., Ltd. (Beijing, China).

Deionized (DI) water from a Millipore Q water purification system was used throughout all experiments. All other chemicals were of analytical grade.

Preparation of g-[C.sub.3][N.sub.4] and g-[C.sub.3][N.sub.4]/PEDOT Nanoporous Composite

g-[C.sub.3][N.sub.4] was prepared by direct heating melamine in an alumina crucible with a cover according to literature [28]. Gold electrodes (2 mm in diameter) were pretreated to a mirror finish with 0.3 and 0.5 pm alumina slurry, rinsed with absolute alcohol and DI water thoroughly, cleaned in an ultrasonic bath for 5 min, and finally dried at room temperature. 3 [micro]L of g-[C.sub.3][N.sub.4] dispersion was drop-coated on the Au electrode surface and dried at ambient temperature. PEDOT was potentiostatically polymerized at 0.8 V (vs. saturated calomel electrode, SCE) for 400 s from a homogeneous aqueous solution containing 0.02 M EDOT monomer and 0.2 M PSS as dopant in a three-electrode cell. The working electrode was the g-[C.sub.3][N.sub.4] coated electrode while the counter and reference electrodes were platinum wire and SCE, respectively. By adjusting the electropolymerization time, the polymer film thickness was controlled. The preparation procedures of the control, the graphene/PEDOT electrode, were the same as those of the g-[C.sub.3][N.sub.4]/PEDOT electrode, except that the drop-coated material was replaced by graphene.

Characterizations

The surface morphology of the coated electrodes was observed by a field emission scanning electron microscope (FESEM, JSM-7600F, Japan), with a voltage of 10 kV. The samples were prepared on small pieces of glass slides. To tell the elemental distribution in the composite, energy dispersive spectroscopy (EDS) was recorded using FESEM. Confocal images of the cultured cells were obtained with a laser confocal imaging system (Nikon TI-E-A1R, Japan).

Electrochemical performances of the modified electrode were investigated by cyclic voltammetry (CV) and electrochemical impedance spectroscopy (EIS) (CHI660D, CH Instruments, Chenhua Inc., Shanghai, China). CV was conducted in a potential scanning range from -0.4 to 0.6 V, with a scan rate of 100 mV/s. EIS was performed in PBS (pH = 7.4) over a wide range of frequencies from 1 to [10.sup.5] Hz with an initial potential of 0.096 V, using an alternating current sinusoid of 5 mV in amplitude. A three-electrode system was employed consisting of a surface modified Au working electrode, a platinum wire counter electrode and a SCE reference electrode. The measurements were repeated three times to obtain the relative standard deviation (RSD) and the data are reported as the mean [+ or -] RSD. All experiments were conducted at ambient temperature. ZSimpWin software (Scriber Associates, Inc.) was employed for the curve fitting analyses.

Neural Cell Culture and MTT Testing

The g-[C.sub.3][N.sub,4]/PEDOT coated cover slips were fixed onto the surface of 24-well culture plates, sterilized with UV light for 5 h, and washed with sterile PBS before cell culture. PC 12 cells were maintained in each well in a nutrient medium composed of DMEM, heat-inactivated fetal bovine serum (10% volume), heat-inactivated horse serum (5%), l-glutamine (2 mM), streptomycin (100 mg/mL), and penicillin (100 units/mL) before incubation in a C[O.sub.2] (5%) and [O.sub.2] (95%) atmosphere. The medium was changed every 2 to 3 days. The cells were cultured for at least 3 days to ensure that all the cells were tightly attached to the substrate surface for further multiplication.

For SEM observation, the cells were treated with 2.5% glutaraldehyde for 2 h. After washing with PBS, the cells were dehydrated in 30% and 50% ethanol in PBS, 70% and 90% ethanol in water, and 100% absolute ethanol in sequence for 15 min, respectively. Finally, the cells were soaked in HMDS for 20 min.

PC 12 cells growing on the g-[C.sub.3][N.sub.4]/PEDOT surfaces were fixed in 4% paraformaldehyde PBS solution for 20 min and washed three times with PBS. The cover slips were immersed in a mixed solution of 5% goat serum and 0.2% triton X-100 in PBS for 1 h. After rinsing with PBS, the cells were incubated in monoclonal antibody against [beta]-III-tubulin (TuJl, 1:250, Beyotime) at 4[degrees]C overnight. Finally, the cells were incubated in a secondary antibody in Alexa Fluor 488 (1:500, Beyotime) for 2 h before laser confocal imaging. PC 12 cells were grown on the graphene/PEDOT surface with the same procedures for comparison.

MTT was dissolved in PBS (pH 7.4) to a concentration of 5.0 g/L and stored at -20[degrees]C. PC 12 cells were cultured on the slips in 400 [micro]L media per well in a 24-well plate, leaving eight wells empty for blank controls. The cells were incubated overnight (37[degrees]C, 5% C[O.sub.2]) to ensure their attachment to the wells. MTT solution was added into the wells followed by incubation at 37[degrees]C for another 4 h. 400 [micro]L DMSO was added to each well and the mixture was placed on a shaking table for 5 min (150 rpm). The absorbance of the suspension was recorded with a microplate reader at 490 nm.

RESULTS AND DISCUSSION

Surface Morphology

Creating a nanoscaled rough surface is crucial for high-performance neural electrodes. To identify the surface morphology of the g-[C.sub.3][N.sub.4]/PEDOT coated electrode, SEM observation was performed and it revealed a rough and porous morphology consisting of small nodules with an average dimension of ~100 nm over the whole area (Fig. la). Such nanoscaled morphology is obviously beneficial for increasing the contact area between the electrode and brain tissue, compared to the flat surface of the planar Au electrodes. Further, graphene/PEDOT was prepared as control and its surface morphology is shown in Fig. lb. It is clearly seen that graphene/PEDOT exhibits bulky sheet morphology. The average area of the convex part is about 0.02 [micro][m.sup.2] for g-[C.sub.3][N.sub.4]/PEDOT and about 0.08 [micro][m.sup.2] for graphene/PEDOT, indicating a much more porous structure of the former nanocomposite.

EDS was applied to confirm the components in the composite. In the spectrum of PEDOT (Fig. 2; left), its component elements of C, O, and S are clearly observed. The spectrum of the composite exhibits an additional peak characteristic of N element in the g-[C.sub.3][N.sub.4] filler (other peaks in the EDS are noise coming from the substrate). It is worth noting that the homogeneity of the g-[C.sub.3][N.sub.4]/PEDOT composite is an important factor to ensure its electrochemical properties and stability. In our experiment, the g-[C.sub.3][N.sub.4] was vigorously stirred in DI water to obtain a homogeneous suspension and the suspension was evenly drop-added onto the entire electrode surface. EDS mapping spectra of C and N were also recorded to give information on the element distribution on the electrode surface. From the mapping spectra (Fig. 2; right) we can see that the N element from g-[C.sub.3][N.sub.4] is uniformly distributed in the PEDOT matrix, demonstrating the homogeneity of the composite.

Electrochemical Properties and Long-Term Stability

The optimal neural electrodes applied to both stimulating and recording devices require low impedance and close coupling between the neural tissue and electrode surface. Low impedance helps reduce the overall power consumption of the devices as well as improve the signal-to-noise ratio [29]. To achieve the best electrochemical properties, it is of necessity to optimize the formulation of g-[C.sub.3][N.sub.4]/PEDOT, including the concentration of g-[C.sub.3][N.sub.4] suspension and electropolymerization time of PEDOT.

EIS provides information on charge transfer characteristics of the surface coating. Most commonly, the impedance value at 1 kHz is specifically examined since most neural communications occur around 1 kHz [30], Figure 3a shows the variation of impedance at 1 kHz with the concentration of g-[C.sub.3][N.sub.4] suspension. We noted that the filled composite material exhibited a nonlinear decrease of the electrical impedance as a function of the filler concentration. When fixing the PEDOT polymerization time, the Z modulus of the g-[C.sub.3][N.sub.4]/PEDOT coating rapidly decreased with g-[C.sub.3][N.sub.4] concentrations from 150 to 350 [micro]g/mL, reached a minimum value, and gradually increased with concentrations up to 450 [micro]g/mL instead. The minimum impedance value might be associated with percolation threshold. At this concentration, g-[C.sub.3][N.sub.4] is able to form a network with PEDOT matrix and the obtained g-[C.sub.3][N.sub.4]/PEDOT coating can provide the largest specific surface area and the most electrical paths for electrons to transport. The electron conduction can take place via tunneling between thin PEDOT layers surrounding the filler particles, leading to a sudden rise of the electrical conductivity, related to the minimum impedance of the composite [31, 32],

Similar to the variation trend in Fig. 3a-c tell us that Z decreased with PEDOT electropolymerization time from 100 to 500 s, reached the minimum value, and increased with polymerization time up to 600 s. The phenomenon can be explained by the fact that PEDOT, with its inherent porous microstructure, provides more active electrical sites to react with ions in the electrolyte. Obviously, a too thick PEDOT coating would decrease its own surface area as well as block the micropores in a g-[C.sub.3][N.sub.4] coating, leading to decrease in surface area and in turn increase the impedance of the nanocomposite.

To confirm the advantage of g-[C.sub.3][N.sub.4]/PEDOT, EIS of the other three materials were conducted for comparison (Fig. 4a). It is reasonable that the impedance of g-[C.sub.3][N.sub.4] or graphene is higher than that of their composites with PEDOT, respectively. Both g-[C.sub.3][N.sub.4] and graphene are electronically conductive materials. Conducting polymers, however, are both electronically and ionically conductive. This feature makes the ions in the electrolyte move in and out of the coating more easily, resulting in greatly decreased impedance of the coating. Hence, PEDOT and its nanocomposites are ideal electrode materials applied in the physiological environments.

EIS can be used for further analysis of the electrochemical properties. Z can be expressed as Z = [absolute value of Z][e.sup.i[theta]], where [absolute value of Z] is the modulus and [theta] is the phase angel. To assess the interfacial properties of the electrodes, Z was studied by using ZSimpWin software. Z data were used for circuit analogs and the simulated circuit is shown in Fig. 4b. For the composites of g-[C.sub.3][N.sub.4]/ PEDOT and graphene/PEDOT, the analog is composed of an uncompensated electrolyte resistance [R.sub.s], a double layer capacitance Cdl, and a charge transfer resistance [R.sub.ct]. Further, the experimental results were fitted to the model and the parameters were calculated using ZSimpWin software (Table 1). In comparison with graphene/PEDOT, g-[C.sub.3][N.sub.4]/PEDOT possesses lower [R.sub.s] and [R.sub.ct], resulting in lower impedance, which is in agreement with the results shown in Fig. 4a. Interestingly, we see that [C.sub.dl] of g-[C.sub.3][N.sub.4]/PEDOT is much higher than that of graphene/ PEDOT, indicating that the former composite has higher CSC values. Again, it demonstrates that g-[C.sub.3][N.sub.4]/PEDOT possesses larger surface area, which plays an important role in determining the electrochemical functionalities of the composite.

The CSC characteristics of the modified electrodes were also explored using CV as shown in Fig. 5a. Amongst the four materials, g-[C.sub.3][N.sub.4]/PEDOT exhibits a well-defined shape with the largest enclosed area. It is known that the integration of I(t) within the cycled region tells the charge capacity of the coated electrode and the enclosed area of the CV trace is proportional to CSC [11]. The result confirms the [C.sub.dl] data in Table 1.

To further evaluate the reversibility of the reactions occurring at the neural interface as well as the long-term electrochemical stability of g-[C.sub.3][N.sub.4]/PEDOT, the g-[C.sub.3][N.sub.4]/PEDOT modified electrode was subjected to 0-500 sweeping cycles at a scan rate of 0.1 V/s, with graphene/PEDOT as control. As displayed in Fig. 5b, the CSC of both electrodes initially decreased, with that of g-[C.sub.3][N.sub.4]/PEDOT declining at a lower rate, and finally stabilized around 450 cycles. g-[C.sub.3][N.sub.4] is an n-type semiconductor with a bandgap of 2.7 eV working in the visible spectral region. Its conjugated structure may offer multiple coupling configurations with conducting polymers, ensuring equivalent efficiency of charge transfer with different PEDOT surfaces, helping keep the stability of g-[C.sub.3][N.sub.4]/PEDOT during cyclic sweeping.

Biocompatibility

Another important factor for materials used for bioapplications is their biocompatibility to ensure safety. Due to their morphological similarity to neurons, PC 12 cells were selected to culture on the g-[C.sub.3][N.sub.4]/PEDOT modified surface. The cell growth and differentiation were monitored by confocal and SEM imaging. As seen in the confocal image (Fig. 6a), the PC 12 cells grew robustly and evenly over the entire g-[C.sub.3][N.sub.4]/ PEDOT coating and were well differentiated with axon outgrowth to form neural networks. Observation with SEM (Fig. 6b) confirms that PC 12 cells were tightly attached to the g[C.sub.3][N.sub.4]/PEDOT surface and presented long neurite extensions, indicating that g-[C.sub.3][N.sub.4]/PEDOT is a promising material for the construction of neural interface. From Fig. 6c we can see that, the same as on the g-[C.sub.3][N.sub.4]/PEDOT surface, the PC 12 cells were well attached and grew with axon outgrowth on graphene/PEDOT surface. The slight difference of cell survival percentage was revealed in Fig. 6d. MTT assay was performed to quantitatively evaluate the cytotoxicity of the g-[C.sub.3][N.sub.4]/ PEDOT modified electrodes. Metabolically active cells can form dark red formazan upon exposure to MTT, thus cell survival is directly proportional to the amount of formazan produced, which is quantified by the UV absorbance at 490 nm. Figure 6d shows the cell viability on the three different surfaces. Slightly more PC 12 cells survived on the g-[C.sub.3][N.sub.4]/PEDOT covered surface, compared with those on the graphene/PEDOT surface. Cell viability on g-[C.sub.3][N.sub.4]/PEDOT was almost as high as that on the blank slip, indicating the negligible cytotoxicity of g-[C.sub.3][N.sub.4]/PEDOT. In combination with the above cell images, we draw a conclusion that g-[C.sub.3][N.sub.4]/PEDOT is a promising candidate material for the surface modification of neural electrodes.

CONCLUSIONS

The developed nanoporous composite of g-[C.sub.3][N.sub.4]/PEDOT exhibits better properties in comparison with its component materials. The porous nanostructure and inherent electroconductivity of both g-[C.sub.3][N.sub.4] and PEDOT confer the composite a larger specific surface area and more electrical paths, facilitating the electrical charge in the electrolyte to move in and out of the composite coating. The synergistic effects result in lower interfacial impedance, higher CSC, and better long-term stability. Moreover, in vitro cell culture demonstrates the excellent biocompatibility and low cytotoxicity of the new nanocomposite, which is crucial for materials used in biological environments. Our study puts forward a new candidate material for the surface modification of implantable neural prosthetic devices.

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Yinghong Xiao [iD], (1,2) Xue Chen, (1) Tongxin Wang, (2) Xiaodi Yang, (1) James Mitchell (2)

(1) Department of Polymeric Materials, Jiangsu Collaborative Innovation Center of Biomedical Fun0ctional Materials, School of Chemistry and Material Science, Nanjing Normal University, Nanjing 210046, People's Republic of China

(2) Nanomaterials Center, College of Dentistry and College of Engineering, Howard University, Washington, DC 20059

Correspondence to: T. Wang; e-mail: twang@howard.edu

Contract grant sponsor: National Natural Science Foundations of China; contract grant number: 21575067; contract grant sponsors: The Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and NIH/NIDCR; contract grant number: ROI DE021786; contract grant sponsor: US Army; contract grant number: W911NF-15-1-0051.

DOI 10.1002/pen.24742

Published online in Wiley Online Library (wileyonlineIibrary.com).

Caption: FIG. 1. SEM images of g-[C.sub.3][N.sub.4]/PEDOT (a) and graphene/PEDOT (b).

Caption: FIG. 2. EDS of PEDOT and g-[C.sub.3][N.sub.4]/PEDOT composite (left) and mapping spectra of C and N in the composite (right). [Color figure can be viewed at wileyonlinelibrary.com]

Caption: FIG. 3. Effect of the concentration of g-[C.sub.3][N.sub.4] suspensions on the impedance at 1 kHz. The inset is the EIS in a frequency range from [10.sup.2] and [10.sup.5] Hz (a). EIS of the g-[C.sub.3][N.sub.4]/PEDOT electrodes with different PEDOT polymerization time (b). The magnified plot of b (c). [Color figure can be viewed at wileyonlinelibrary.com]

Caption: FIG. 4. EIS of g-[C.sub.3][N.sub.4], graphene, g-[C.sub.3][N.sub.4]/PEDOT and graphene/PEDOT (a). Circuit analog of the impedance data for the nanocomposites (b). [Color figure can be viewed at wileyonlinelibrary.com]

Caption: FIG. 5. CVs of g-[C.sub.3][N.sub.4], graphene, g-CjN^EDOT, and graphene/PEDOT (a). Evaluation of stability of g-[C.sub.3][N.sub.4]/ PEDOT and graphene/PEDOT coatings over 500 cycles at a scan rate 0.1 V/s for repeating electrochemical excitation (b). [Color figure can be viewed at wileyonlinelibrary.com]

Caption: FIG. 6. Confocal (a) and SEM image (b) of PC 12 cells cultured on g-[C.sub.3][N.sub.4]/PEDOT surface. Confocal image of PC12 cells cultured on graphene/PEDOT surface (c). MTT quantitative analysis of PC12 cell viability (d). [Color figure can be viewed at wileyonlinelibrary.com]
TABLE 1. EIS parameters of the g-[C.sub.3][N.sub.4]/PEDOT and
graphene/PEDOT composites by fitting the experimental data to the
equivalent circuit model.

Nanocomposite                  [R.sub.2]     [C.sub.dl]    [R.sub.ct]
                                ([ohm])      ([micro]F)      (k[ohm])

g-[C.sub.3][N.sub.4]/PEDOT       24.66         300.9          16.02
Graphene/PEDOT                   28.66         168.5          21.72
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Author:Xiao, Yinghong; Chen, Xue; Wang, Tongxin; Yang, Xiaodi; Mitchell, James
Publication:Polymer Engineering and Science
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Date:Sep 1, 2018
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