High-resolution mapping of infraslow cortical brain activity enabled by graphene microtransistors

Eduard Masvidal-Codina, Xavi Illa, Miguel Dasilva, Andrea Bonaccini Calia, Tanja Dragojević, Ernesto E. Vidal-Rosas, Elisabet Prats-Alfonso, Javier Martínez-Aguilar, Jose M. De la Cruz, Ramon Garcia-Cortadella, Philippe Godignon, Gemma Rius, Alessandra Camassa, Elena Del Corro, Jessica Bousquet, Clement Hébert, Turgut Durduran, Rosa Villa, Maria V. Sanchez-Vives, Jose A. Garrido, Anton Guimerà-Brunet. Nature Materials (2018). Published: 31 December 2018. DOI: 10.1038/s41563-018-0249-4

Recording infraslow brain signals (<0.1 Hz) with microelectrodes is severely hampered by current microelectrode materials, primarily due to limitations resulting from voltage drift and high electrode impedance. Hence, most recording systems include high-pass filters that solve saturation issues but come hand in hand with loss of physiological and pathological information. In this work, we use flexible epicortical and intracortical arrays of graphene solution-gated field-effect transistors (gSGFETs) to map cortical spreading depression in rats and demonstrate that gSGFETs are able to record, with high fidelity, infraslow signals together with signals in the typical local field potential bandwidth. The wide recording bandwidth results from the direct field-effect coupling of the active transistor, in contrast to standard passive electrodes, as well as from the electrochemical inertness of graphene. Taking advantage of such functionality, we envision broad applications of gSGFET technology for monitoring infraslow brain activity both in research and in the clinic. © 2018, The Author(s), under exclusive licence to Springer Nature Limited.

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Dexamethasone Reduces the Foreign Body Reaction to Intraneural Electrode Implants in the Peripheral Nerve of the Rat

De la Oliva N., Navarro X., del Valle J. Anatomical Record301 (10): 1722 – 1733. 2018. 10.1002/ar.23920. IF: 1.373

Intraneural electrodes must be in intimate contact with nerve fibers to have a proper function, but this interface is compromised due to the foreign body reaction (FBR). The FBR is characterized by a first inflammatory phase followed by a second anti-inflammatory and fibrotic phase, which results in the formation of a tissue capsule around the implant, causing physical separation between the active sites of the electrode and the nerve fibers. We have tested systemically several anti-inflammatory drugs such as dexamethasone (subcutaneous), ibuprofen and maraviroc (oral) to reduce macrophage activation, as well as clodronate liposomes (intraperitoneal) to reduce monocyte/macrophage infiltration, and sildenafil (oral) as an antifibrotic drug to reduce collagen deposition in an FBR model with longitudinal Parylene C intraneural implants in the rat sciatic nerve. Treatment with dexamethasone, ibuprofen, or clodronate significantly reduced the inflammatory reaction in the nerve in comparison to the saline group after 2 weeks of the implant, whereas sildenafil and maraviroc had no effect on infiltration of macrophages in the nerve. However, only dexamethasone was able to significantly reduce the matrix deposition around the implant. Similar positive results were obtained with dexamethasone in the case of polyimide-based intraneural implants, another polymer substrate for the electrode. These results indicate that inflammation triggers the FBR in peripheral nerves, and that anti-inflammatory treatment with dexamethasone may have beneficial effects on lengthening intraneural interface functionality. Anat Rec, 301:1722–1733, 2018. © 2018 Wiley Periodicals, Inc. © 2018 Wiley Periodicals, Inc.

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Photocurrent generation of biohybrid systems based on bacterial reaction centers and graphene electrodes

Csiki R., Drieschner S., Lyuleeva A., Cattani-Scholz A., Stutzmann M., Garrido J.ADiamond and Related Materials89: 286 – 292. 2018. 10.1016/j.diamond.2018.09.005.

The direct conversion of sunlight into chemical energy via photosynthesis is a unique capability of plants and some bacterial species. Aimed at mimicking this energy conversion process, the combination of inorganic substrates and organic photoactive proteins into an artificial biohybrid system is of a great interest for artificial bio-photovoltaic applications. It also allows to better understand charge transfer processes involved in the photosynthetic chain. In this work, single layer graphene (SLG) and multilayer graphene (MLG) electrodes are used as a platform for the immobilization of reaction centers (RCs) from purple bacteria Rhodobacter sphaeroides, a protein complex responsible for the generation of photo-excited charges.

Electrochemical experiments with graphene electrodes and redox molecules reveal fundamental differences in the charge transfer processes for SLG and MLG films. We demonstrate that both graphene-based materials enable the immobilization of RCs without loss of functionality, attested by a photocurrent generation under illumination with IR-light at a wavelength of 870 nm. Furthermore, we report on the dependence of the generated photocurrent on the applied bias voltage, as well as on the presence of charge mediators in the surrounding electrolyte. This work demonstrates that SLG and MLG are a suitable platform for RC immobilization and subsequent photocurrent generation, suggesting a promising potential for graphene-based materials in bio-photovoltaics. © 2018 Elsevier B.V.

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Understanding the bias dependence of low frequency noise in single layer graphene FETs

Mavredakis N., Garcia Cortadella R., Bonaccini Calia A., Garrido J.A., Jiménez D. Nanoscale10 (31): 14947 – 14956. 2018. 10.1039/c8nr04939d.

This letter investigates the bias-dependent low frequency noise of single layer graphene field-effect transistors. Noise measurements have been conducted with electrolyte-gated graphene transistors covering a wide range of gate and drain bias conditions for different channel lengths. A new analytical model that accounts for the propagation of the local noise sources in the channel to the terminal currents and voltages is proposed in this paper to investigate the noise bias dependence. Carrier number and mobility fluctuations are considered as the main causes of low frequency noise and the way these mechanisms contribute to the bias dependence of the noise is analyzed in this work. Typically, normalized low frequency noise in graphene devices has been usually shown to follow an M-shape dependence versus gate voltage with the minimum near the charge neutrality point (CNP).

Our work reveals for the first time the strong correlation between this gate dependence and the residual charge which is relevant in the vicinity of this specific bias point. We discuss how charge inhomogeneity in the graphene channel at higher drain voltages can contribute to low frequency noise; thus, channel regions nearby the source and drain terminals are found to dominate the total noise for gate biases close to the CNP. The excellent agreement between the experimental data and the predictions of the analytical model at all bias conditions confirms that the two fundamental 1/f noise mechanisms, carrier number and mobility fluctuations, must be considered simultaneously to properly understand the low frequency noise in graphene FETs. The proposed analytical compact model can be easily implemented and integrated in circuit simulators, which can be of high importance for graphene based circuits’ design. © The Royal Society of Chemistry.

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Single-layer graphene modulates neuronal communication and augments membrane ion currents

Pampaloni N.P., Lottner M., Giugliano M., Matruglio A., D’Amico F., Prato M., Garrido J.A., Ballerini L., Scaini D. Nature Nanotechnology13(8): 755 – 764. 2018. 10.1038/s41565-018-0163-6.

The use of graphene-based materials to engineer sophisticated biosensing interfaces that can adapt to the central nervous system requires a detailed understanding of how such materials behave in a biological context. Graphene’s peculiar properties can cause various cellular changes, but the underlying mechanisms remain unclear. Here, we show that single-layer graphene increases neuronal firing by altering membrane-associated functions in cultured cells. Graphene tunes the distribution of extracellular ions at the interface with neurons, a key regulator of neuronal excitability. The resulting biophysical changes in the membrane include stronger potassium ion currents, with a shift in the fraction of neuronal firing phenotypes from adapting to tonically firing. By using experimental and theoretical approaches, we hypothesize that the graphene–ion interactions that are maximized when single-layer graphene is deposited on electrically insulating substrates are crucial to these effects. © 2018, The Author(s).

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Lipid Monolayer Formation and Lipid Exchange Monitored by a Graphene Field-Effect Transistor

Blaschke B.M., Böhm P., Drieschner S., Nickel B., Garrido J.A. Langmuir34 (14): 4224 – 4233. 2018. 10.1021/acs.langmuir.8b00162.

Anionic and cationic lipids are key molecules involved in many cellular processes; their distribution in biomembranes is highly asymmetric, and their concentration is well-controlled. Graphene solution-gated field-effect transistors (SGFETs) exhibit high sensitivity toward the presence of surface charges. Here, we establish conditions that allow the observation of the formation of charged lipid layers on solution-gated field-effect transistors in real time. We quantify the electrostatic screening of electrolyte ions and derive a model that explains the influence of charged lipids on the ion sensitivity of graphene SGFETs. The electrostatic model is validated using structural information from X-ray reflectometry measurements, which show that the lipid monolayer forms on graphene. We demonstrate that SGFETs can be used to detect cationic lipids by self-exchange of lipids. Furthermore, SGFETs allow measuring the kinetics of layer formation induced by vesicle fusion or spreading from a reservoir. Because of the high transconductance and low noise of the electrical readout, we can observe characteristic conductance spikes that we attribute to bouncing-off events of lipid aggregates from the SGFET surface, suggesting a great potential of graphene SGFETs to measure the on-off kinetics of small aggregates interacting with supported layers. © 2018 American Chemical Society.

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