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Akbari, M.K.;  Lopa, N.S.;  Shahriari, M.;  Najafzadehkhoee, A.;  Galusek, D.;  Zhuiykov, S. Carbon Based Two-Dimensional Materials for Bioelectronic Neural Interfacing. Encyclopedia. Available online: https://encyclopedia.pub/entry/40631 (accessed on 07 July 2024).
Akbari MK,  Lopa NS,  Shahriari M,  Najafzadehkhoee A,  Galusek D,  Zhuiykov S. Carbon Based Two-Dimensional Materials for Bioelectronic Neural Interfacing. Encyclopedia. Available at: https://encyclopedia.pub/entry/40631. Accessed July 07, 2024.
Akbari, Mohammad Karbalaei, Nasrin Siraj Lopa, Marina Shahriari, Aliasghar Najafzadehkhoee, Dušan Galusek, Serge Zhuiykov. "Carbon Based Two-Dimensional Materials for Bioelectronic Neural Interfacing" Encyclopedia, https://encyclopedia.pub/entry/40631 (accessed July 07, 2024).
Akbari, M.K.,  Lopa, N.S.,  Shahriari, M.,  Najafzadehkhoee, A.,  Galusek, D., & Zhuiykov, S. (2023, January 31). Carbon Based Two-Dimensional Materials for Bioelectronic Neural Interfacing. In Encyclopedia. https://encyclopedia.pub/entry/40631
Akbari, Mohammad Karbalaei, et al. "Carbon Based Two-Dimensional Materials for Bioelectronic Neural Interfacing." Encyclopedia. Web. 31 January, 2023.
Carbon Based Two-Dimensional Materials for Bioelectronic Neural Interfacing
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This entry is adapted from the peer-reviewed paper 10.3390/jfb14010035

Realizing the neurological information processing by analyzing the complex data transferring behavior of populations and individual neurons is one of the fast-growing fields of neuroscience and bioelectronic technologies. This field is anticipated to cover a wide range of advanced applications, including neural dynamic monitoring, understanding the neurological disorders, human brain–machine communications and even ambitious mind-controlled prosthetic implant systems. To fulfill the requirements of high spatial and temporal resolution recording of neural activities, electrical, optical and biosensing technologies are combined to develop multifunctional bioelectronic and neuro-signal probes. Advanced two-dimensional (2D) layered materials such as carbon based 2D materials with their atomic-layer thickness and multifunctional capabilities show bio-stimulation and multiple sensing properties. These characteristics are beneficial factors for development of ultrathin-film electrodes for flexible neural interfacing with minimum invasive chronic interfaces to the brain cells and cortex.

two-dimensional materials neural interfacing neural electrodes

1. Garphene

Graphene, the most famous carbon-based two-dimensional (2D) structure, is recognized as a functional material for neural interfacing applications [1]. Its excellent conductivity, mechanical stability, transparency and facile functionalization place graphene in a unique position for applications in neurotechnologies, biosensing and multi-modal neural interfacing [2][3]. Graphene-based 2D materials have been employed either passively or actively as the components of microelectrodes or transistors in neural interfaces. The graphene neural interfaces record either chemical signals, such as the concentrations of neurotransmitters, or measure electrical indicators, such as local field potentials. 
High-temporal-resolution recording of neuron cell activities is one of the main targets of electrophysiology, where optical and cellular imaging techniques are accompanied by electrophysiological signal recordings to complement the performance of each individual technique and then provide a clear image of the neurological behavior [4][5][6]. However, conventional metal microelectrodes cannot be employed in cellular imaging techniques due their shadow and blockage effects [7][8]. Furthermore, light-induced effects on the metal components adversely interfere in the potential signal recording process. These limitations can be overcome by the development of transparent 2D graphene microelectrodes, where the optical transparency of the graphene-based neural interface enables cellular imaging and electrophysiological recording [9]. Different synthesis methods for 2D graphene provide various types of 2D nanostructures. Chemical vapor deposition (CVD) graphene [10], few-layer exfoliated graphene, and chemically synthesized graphene all have different physical and chemical characteristics. The availability of various 2D graphene nanostructures with distinct properties and doping capabilities have opened up outstanding opportunities for the development of neural interfaces. Graphene field-effect transistors (GFETs) [11] are another electronic system developed for neural interfacing applications. GFETs have interesting applications in bioelectronic systems.

1.1. Graphene Microelectrodes

Fluorescence microscopy can be combined with invasive graphene-based microelectrodes to visually depict the precise active location of neural signals [7]. Calcium imaging with fluorescence response cannot resolve the high-frequency spikes of large populations of neural cells, while the presence of graphene-based neural interface electrodes enabled the detection of high-frequency neural reactions [7]. A study investigated the simultaneous electrophysiological recording of neural responses via invasive transparent graphene-based neural interface electrodes. The results were later combined with optical fluorescence imaging. This approach incorporated the advantages of temporal and spatial resolution of both electrophysiological recording and imaging techniques. Such an approach ensures detection of the internal and ictal activities, and also guarantees the successful monitoring of ultra-fast neural spikes (5 ms) and population discharges, which are not possible to track by using merely the multicellular calcium imaging technique [9]. This developed graphene-based microelectrode system also demonstrated a six-fold improvement in the signal-to noise-ratio (SNR) value and 100-fold reduction of electrical interference noise [9]. Similar results were also reported by another study where electrical recording synchronized with wide-field calcium imaging was combined for investigation of the local neural activities of cortical modules [9]. A comparison of interictal-like spiking activities recorded by Au and graphene electrodes confirmed that the noise level in the doped graphene electrodes was almost six times lower than that of Au electrodes, while the impedance levels remained comparable at a signal frequency of 1 kHz. Subsequent comparisons showed the suppression of electrical interference noise in doped graphene electrodes. This confirmed that graphene has a clear advantage for the study of brain activities at low local-field potential ranges (1–100 Hz), which are a property of information pulses and synaptic potential signals at low frequencies. Another study employed four-layer chemical vapor-deposited (CVD) graphene films on transparent invasive electrode arrays to successfully monitor neural activities in a mouse neural system expressing channelrhodopsin-2 under blue light stimulation [12]. Transparency and thickness were two interrelated factors that already affected the impedance values of optically stimulated neural interfaces in this study [13]. By the careful design of transparent graphene electrodes (number of layers), it was possible to tackle the challenges stemming from the light-induced problems to achieve local-field potential recording of neural activities via optogenetics stimulation [14]. For example, the graphene monolayer is transparent, but its impedance is relatively high compared with that of other types of conventional porous structures and metal faradic interfaces. The proposed mechanism for the impedance reduction was an alteration of graphene surface characteristics by nitric acid (up to almost 50%) [11][15]. Furthermore, there are always trade-offs among the electrode footprint, SNR, and interference impedances at the neural interfaces. An increase in contacting interfaces can facilitate the capture of a higher number of ionic species transferred at the heterointerface between the graphene electrode and extracellular spaces. Despite the numerous desirable characteristics of graphene monolayer for neural interfacing, the intrinsic capacity of graphene monolayer for charge injection is still not sufficient for the efficient electrical stimulation of neurons. It was suggested that porous three-dimensional (3D) structures of graphene nanosheet electrodes can efficiently demonstrate high capacity for charge injection at the neural interfaces and at the same time present reasonably low heterointerface impedance [16]. Favorably, the fabrication of 3D porous graphene-based electrodes with polymer coatings considerably enhanced the mechanical stability and reduced the impedance of neural interfaces [17].
As an example, porous graphene nanostructures were grown on polyamide substrate by laser pyrolysis [16]. This approach enabled the fabrication of highly adhesive 3D graphene nanosheets with considerable mechanical stability of electrodes for neural interfacing applications (over one million cyclic operations) [16]. A high charge capacitance value of 3.1 mC cm−2 was recorded for a 3D graphene-based electrode that was employed for in vivo stimulation of motor cortex arrays of mouse leg [16]. In this setup, porous graphene electrodes containing 16-electrode arrays of graphene whiskers were employed by a pair of needle electrodes to stimulate the motor cortex of mouse brain with electrical pulses. These electrical signals evoked transient knee and ankle flexion in contralateral mouse legs. The corresponding electrical current response of the system was measured and recorded. A direct relation was found between the amplitude of the stimulus current and the movement response of knee and ankle, confirming the capability of the developed penetrating porous graphene electrode arrays as minimally invasive neural interfaces for the brain–computer interface and neural prosthesis applications [16]. In particular, the distinctive capacitive characteristics of fabricated 3D graphene arrays tangibly eliminated the corrosion-related risks that are recognized as critical challenges in faradic electrodes.

1.2. Graphene Field-Effect Transistors (GFETs)

In parallel with microelectrodes, GFETs are being developed for a wide range of biosensing applications, where the transduction of biological signals is amplified locally due to the strong field effects induced [18][19][20][21]. The main advantage of GFET configurations compared to graphene microelectrodes stems from the impact of intrinsic amplification on the SNR factor of neural interfaces. A GFET works on the basis of the interaction of 2D graphene gate material with the electrolyte solution. A study was conducted on the visual part of brain cortex where GFET neural interfaces were employed for measurements. In this study, SNR values of 62 for pre-epileptic activities and 9.8 for spontaneous oscillation were achieved [22]. Similar values for Pt electrodes were, respectively, 53 and 8.33 for in vivo recording [22]. In another recent study, a monolayer graphene gate was developed by chemical vapor deposition to be in contact with brain tissue where the gate bias voltage was applied via a reference electrode [20]. The presence and concentration of charge carriers at the neural interfaces on brain tissue can alter the conductivity of the graphene gate upon the application of gate voltages at the graphene-electrolyte heterointerfaces. Therefore, planar arrays of 2D graphene were developed on the transparent substrate [20]. These multi-neural probes were assembled on the rat’s brain tissue for mapping targets. In this setup, the GFET arrays could continuously provide mapping images from the epicortical brain activities for 24 h by monitoring patterns of responses to infra-slow fluctuations (ISFs) [20][21]. Infra-slow oscillation of electroencephalogram (EEG) signals refers to specific brain signals with frequencies in the range of 0.01 and 0.1 Hz. The neural interfaces were composed of non-invasive graphene array electrodes positioned on the cortex of a rat, where an Ag/AgCl reference electrode and two individual Pt-Ir electrodes were accompanied by GFET arrays. Informative signals extracted from coupled channels from the neural interface were accompanied by corresponding mapping at ultra-low frequencies (~1 MHz). The results confirmed the capability and maturity of this Internet of Things (IoT) technology for online, long-term and consistent monitoring of brain activities through in vitro and in vivo evaluations of neural signals [21].

2. Other Types of Graphene-Based Materials

The availability of various types of graphene-based materials, including single-layer CVD films, multilayered exfoliated films, and chemically and mechanically synthesized films, has enabled the development of various types of graphene-based neural interfaces. Despite the fact that a large number of bioresearch activities have been devoted to graphene, the high hydrophobicity of pristine graphene has limited its applications. Functionalized graphene, graphene oxide (GO) and reduced graphene oxide (rGO) 2D structures can be valuable alternatives to graphene in neural interfaces. Two-dimensional GO is an atomically thin structure where oxidation enables the incorporation of oxygen functional groups into the surface of the graphene, thus decreasing the graphene aggregation in aqueous solutions as well as reducing its electrical conductivity. Recently, ultra-large graphene oxide flakes were deposited on binder-free microfibers to replace conventional filament-shaped metallic invasive neural electrodes [8][9]. In these GO-based microfiber sensors, the specific contact impedance was improved to a lower value (3.9 MΩ μm−2 at the 1 kHz frequency), while it showed considerably better charge storage capacity (361 ± 45 mC cm−2) compared with that of the conventional metallic-based filament microelectrodes used in neural interfacing systems. Similar research studies also included graphene as the main sensing component in microfibers [23][24].
Despite its greater functionalization capabilities, GO has highly restricted electron mobility on its surface. GO is technically an insulator; therefore, reduction reactions are carried out to partially remove oxygen and then alter or recover the electrical conductivity of 2D GO films. Consequently, reduced graphene oxide (rGO) with higher conductivity is extensively employed for biosensing and especially non-invasive neural interfacing applications. Typically, 2D rGO nanostructures are developed or grown during the fabrication process for neural interfaces at the heterointerfaces between the sensing components, which in turn facilitate swift charge transfer and low contact impedance at the neural interfaces. Non-invasive graphene-based polymer wearable sensors are well-developed for the characterization and precision sensing of biosignals with high levels of accuracy [25][26][27]. One of the main and widely available polymer substrates for fabrication of non-invasive thin-film wearable electronic neural interfaces is polydimethylsiloxane (PDMS). Various conductive layers can be developed on the PDMS layers by electrospinning, sputtering and spray coating to fabricate the skin-mounting side of the neural interfaces. There are several reports of successful performance of graphene-based wearable and flexible neural interfaces, where GO and rGO were employed as the main components of the sensors. In one study, neural interfaces were composed of patterned rGO films developed from chemically treated GO nanosheets. This setup showed considerable low contact impedance of 500 kΩ at a signal frequency of 50 Hz [12]. In another example, rGO-based neural interfaces were developed on PDMS substrates through laser-assisted GO reduction. These flexible non-invasive sensors demonstrated ultra-low skin impedance of ~60 kΩ at 10 Hz [28]. Another rGO/nylon epidermal sensor was fabricated by the hydrothermal synthesis of GO, followed by its thermal reduction to rGO films. Such conductive sensors with low on-skin impedance of 15 kΩ at 100 Hz were used for non-invasive monitoring of electrocardiography (ECG) and electromyography (EMG) signals [29]. Another type of non-invasive neural interface are E-skins, which are soft and flexible epidermal electronic devices with multifunctional applications. Graphene and its family were extensively employed for the fabrication of tattoo sensors for the reception and sensing of vital neural and physical signs [30][31][32]. Specifically, e-tattoos based on the 2D graphene family with nanomesh structures [33] and CVD graphene [34] provided considerably low resistance (~24 Ω/sq) for precise reception and long-term monitoring of brain activities (EEG) and sleep monitoring. In this setup, optimized dry electrodes were fabricated by CVD of graphene layers with thickness of 100 nm on PEDOT:PSS electrodes (PTG). These electrodes exhibited high levels of conductivity attributable to their graphene layers (4142 S/cm), high optical transparency and mechano-electrical stability for e-skin bioelectronic applications [35]. Optical transparency enabled incorporation of the outcomes of laser speckle contrast imaging into EEG and EMG measurements. This process was highly beneficial for the deep understanding of pathological process mechanisms. The developed PTG sensors successfully recorded EEG signals in the sleeping, exercising and relaxing states.
Due to the facile dispersion of GO and rGO, these structures can be feasibly used for the fabrication of fiber neural interfaces. In such development, the fibers (nylon, cotton, polyesters) are dip-coated in GO or rGO dispersions, followed next by thermal treatment. These microfiber neural interfaces showed considerably improved conductivity and low impedance for wearable neural interfacing [35][36][37][38][39]. Monolayer and porous graphene were also employed for free-standing neural interfaces. In one approach, liquid-crystal GO and rGO were used to make microfiber sensors with a high level of charge injection capacity (46 mC cm−2) [39]. These free-standing electrodes based on reduced liquid-crystal GO and porous graphene electrodes successfully stimulated retinal ganglion cells. The incredibly low impedance, high charge injection, storage capacity and high fidelity of these sensors for neural stimulation originated from their large effective surface areas. Improvements in the conductivity of rGO have been extensively investigated to enhance the functionalities of these 2D structures. Chemical treatment is one of the main approaches. As an example, a low-temperature chemical method using hydroiodic acid (HI) and L-ascorbic acid (L-AA) can effectively enhance the conductivity of rGO. While HI and L-AA are known as effective reductants, their combination resulted in improved electrical conductivity of up to 1115 S/m [40]. Another study employed graphene oxide–gold oxide (rGO/Au2O3) nanocomposite electrodes as implantable neural interfaces for applications in electrophysiology and neurochemistry. The rGO/Au2O3-modified electrodes displayed significantly improved activities [41]. Current studies are devoted to improving the functionalities of graphene-based 2D neural interfaces to attain high spatiotemporal resolution signal recording. The majority of existing sensors work on the basis of electrochemical sensing of biosignals. Low heterointerface impedance accompanied by high SNR characteristics are the main requirements for graphene-based neural interfaces. Table 1 provides a brief overview on the neural interfaces fabricated by graphene, GO and rGO 2D materials.
Table 1. Neural interfaces based on 2D carbon-based materials.
Neural Interface Application SNR Impedance Electrode Dimensions Stability Tests Ref.
rGO microarrays developed on PDMS (non-invasive) (e-skin) EEG, EMG, electrooculography (EOG) 16.8 dB ~500 kΩ at 50 Hz N/A 60 times reuse 58 h stability [25]
Laser-induced GO developed on PET (non-invasive) ECG ~70 dB ~60 kΩ at 50 HZ 4 cm2 >100 h [26]
Porous graphene array developed by laser pyrolysis (invasive) Planar electrodes for neural activities N/A 5 kΩ at 1 KHz 250 μm2 106 cycles [16]
Epitaxial graphene films developed on silicon substrate (non-invasive) EEG N/A 68 ± 4 kΩ at 10 Hz 1 cm2 120 days [42]
Doped single-layered graphene (invasive) Planar electrodes for neural activities 40 541 kΩ at 1 KHz 50 × 50 μm2 6 months [7]
Liquid-crystal GO fiber coated with parylene C Filament deep probing N/A 50 kΩ at 1 KHz N/A 14 days [24]
CVD graphene-based transparent microarray (invasive) Optogenetics and neural imaging N/A 243.5 kΩ at 1 KHz 3.1 × 3.1 mm2 70 days implanted [12]
Multielectrode array based on graphene microtransistor (invasive) Neural deep probing N/A N/A N/A 10 weeks implanted [28]
rGO developed on nylon membrane (non-invasive) ECG, EMG N/A ~15 kΩ at 1000 Hz N/A 50 h [29]
Laser-developed graphene on PU nanomesh (non-invasive) EEG, ECG, EOG 14.12 dB N/A 1.5 cm2 1000 cycles [33]
CVD graphene for PMMA tattoo (non-invasive) ECG, EMG, EEG, EOG 15.22 dB ~13 kΩ at 1 KHz 1.225 cm2 N/A [43]
rGO-PEDOT/PSS fabricated on nylon-lycra (non-invasive) ECG 21.6 dB ~50 kΩ at 100 Hz 1 × 1 cm2 50 cycles [44]
Electrospun fiber with graphene monolayer (non-invasive) ECG, EEG, sEMG ~30 dB 150 Ω N/A 10 times [45]
CVD graphene multilayer electrodes developed on parylene Neural interfaces compatible with magnetic resonance imaging (MRI) N/A 27.4 kΩ at 1 KHz 430 μm diameter N/A [46]

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Subjects: Materials Science, Biomaterials
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Mohammad Karbalaei Akbari
,
Nasrin Siraj Lopa
,
Marina Shahriari
,
Aliasghar Najafzadehkhoee
,
Dušan Galusek
,
Serge Zhuiykov
View Times: 311
Revisions: 3 times (View History)
Update Date: 01 Feb 2023
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