Near-infrared excitation of nitrogen-doped ultrananocrystalline diamond photoelectrodes in saline solution

https://doi.org/10.1016/j.diamond.2020.107720Get rights and content

Highlights

  • Near-infrared generates charge in nitrogen doped ultrananocrystalline diamond.

  • Oxygen surface termination results in a capacitive charge coupling.

  • Hydrogen surface termination results in a faradic charge transfer.

  • Oxygen surface termination results in an increased photoresponsivity.

Abstract

Nitrogen-doped ultrananocrystalline diamond (N-UNCD) is a promising material for a variety of neural interfacing applications, due to its unique combination of high conductivity, bioinertness, and durability. One emerging application for N-UNCD is as a photoelectrode material for high-precision optical neural stimulation. This may be used for the treatment of neurological disorders and for implantable bionic devices such as cochlear ear implants and retinal prostheses. N-UNCD is a well-suited material for stimulation photoelectrodes, exhibiting a photocurrent response to light at visible wavelengths with a high charge injection density [A. Ahnood, A. N. Simonov, J. S. Laird, M. I. Maturana, K. Ganesan, A. Stacey, M. R. Ibbotson, L. Spiccia, and S. Prawer, Appl. Phys. Lett. 108, 104,103 (2016)]. In this study, the photoresponse of N-UNCD to near-infrared (NIR) irradiation is measured. NIR light has greater optical penetration through tissue than visible wavelengths, opening the possibility to stimulate previously inaccessible target cells. It is found that N-UNCD exhibits a photoresponsivity which diminishes rapidly with increasing wavelength and is attributed to transitions between mid-gap states associated with the graphitic phase present at the grain boundaries and the conduction band tail. Oxygen surface termination on the diamond films provides further enhancement of the injected charge per photon, compared to as-grown or hydrogen terminated surfaces. Based on the measured injected charge density, we estimate that the generated photocurrent of oxygen terminated N-UNCD is sufficient to achieve extracellular stimulation of brain tissue within the safe optical exposure limit.

Introduction

The use of light-based techniques for neural stimulation is an area of growing interest, with potential applications in the treatment of neurological disorders and in implantable bionic devices [[1], [2], [3], [4]]. In particular, optically-driven electrodes have the potential to offer wireless stimulation with much greater spatial resolution than conventional electrically-driven electrodes [2]. This approach relies on the transduction of light into electrical signals in order to stimulate neural tissue, caused by the separation of photo-excited charge carriers in a semiconducting electrode [2]. Materials such as photoconductive silicon [[5], [6], [7], [8]], conductive polymers [[9], [10], [11]], and quantum dots [[12], [13], [14]] have been extensively studied for this purpose. However, these photoactive surfaces have often been found to exhibit limited biostability or produce cytotoxic reactions [[15], [16], [17], [18], [19], [20]].

Diamond is a material with the potential to address these issues, due to its well-known durability and biocompatibility [[21], [22], [23], [24], [25]]. Single crystal diamond is a wide-gap semiconductor with an intrinsic photoresponse band at unsafe ultraviolet frequencies and hence is not useful for neural stimulation applications. In contrast, nitrogen-doped ultrananocrystalline diamond (N-UNCD) is highly conductive due to the presence of sp2 bonded carbon at the diamond grain boundaries, and has been shown to exhibit a photoresponse at much longer wavelengths [26,27], making it a material well-suited for photostimulation [28]. In addition, the surface chemistry of N-UNCD may be altered to exhibit high electrochemical capacitance, a desirable attribute for neuromodulation electrodes [23,29].

The potential of N-UNCD for use as a photoelectrode material has been previously investigated, with the finding that it exhibits a photoresponse to wavelengths of 450 nm or shorter, meeting the requirements for extracellular and intercellular stimulation within the safe optical exposure limit [28]. In the present study, the feasibility of extending the wavelength range of the photoresponse is investigated. Longer wavelengths have greater optical penetration depth in biological tissue, and reduce the potential for phototoxic effects resulting in higher safe optical exposure limits [19,30]. To test this, the spectral response of N-UNCD is measured and analysed with reference to the known band structure. The effect of the surface chemistry on the electrochemical capacitance and charge transfer mechanisms was also examined. Finally, the capability of this technique to achieve threshold charge injection for the stimulation of neurons is evaluated, taking into account various parameters such as cell type, laser pulse parameters, and the size of the stimulating electrodes.

Section snippets

Experimental

The N-UNCD thin-film samples used in this study were grown in an Iplas microwave plasma-assisted CVD system on polycrystalline diamond (PCD) and nanodiamond-seeded silicon substrates. Films were grown to a thickness of approximately 30 μm. Details of the N-UNCD seeding and deposition processes have been reported elsewhere [23]. Samples underwent further plasma treatment to terminate the surface with either hydrogen or oxygen. The treatment conditions have also been reported in earlier works [23,

Electrochemical properties of N-UNCD

To investigate the suitability of N-UNCD as a photoelectrode material, the electrochemical properties were investigated using cyclic voltammetry and photocurrent measurements for different chemical surface terminations. As shown in Fig. 2(a), the electrochemical capacitance of N-UNCD measured by cyclic voltammetry is highly dependent on the chemical termination of the diamond surface. As-grown and hydrogen terminated N-UNCD samples exhibit similar electrochemical behaviour, with both

Summary and conclusions

In summary, the performance of N-UNCD as an optically-driven electrode for neural stimulation applications was investigated over a range of wavelengths. It was determined that N-UNCD exhibits a sub-bandgap photoresponse which diminishes with increasing wavelength, an effect attributed to transitions between mid-gap defect states associated with the graphitic grain boundary regions. It was also found that oxygen surface termination enhances the photoresponse through a capacitive charge transfer

CRediT authorship contribution statement

Andre Chambers: Formal analysis, Investigation, Methodology, Writing - original draft, Writing - review & editing. Arman Ahnood: Conceptualization, Funding acquisition, Methodology, Writing - original draft, Writing - review & editing, Supervision, Validation, Project administration. Samira Falahatdoost: Methodology. Steve Yianni: Formal analysis, Investigation, Methodology. David Hoxley: Resources. Brett C. Johnson: Resources, Formal analysis. David J. Garrett: Resources. Snjezana

Declaration of competing interest

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: S.P. is a shareholder, director and chief technology officer of iBIONICS. S.P. and D.J.G. are directors and shareholders in Carbon Cybernetics. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgements

This work was performed in part at the Australian National Fabrication Facility (ANFF), a company established under the National Collaborative Research Infrastructure Strategy, through the La Trobe University Centre for Materials and Surface Science. The authors also wish to acknowledge the technical assistance of Dr. Matias Maturana at Clinical Sciences, Department of Medicine, University of Melbourne, as well as helpful discussions with Alastair Stacey and Nikolai Dontschuk from the School of

References (59)

  • T. Kondo et al.

    AC impedance studies of anodically treated polycrystalline and homoepitaxial boron-doped diamond electrodes

    Electrochim. Acta

    (2003)
  • C.E. Nebel et al.

    Persistent photocurrents in CVD diamond

    Diam. Relat. Mater.

    (2000)
  • M. Shaban et al.

    Characterization and design optimization of heterojunction photodiodes comprising n-type ultrananocrystalline diamond/hydrogenated amorphous carbon composite and p-type Si

    Mater. Sci. Semicond. Process.

    (2018)
  • G. Strangman et al.

    Non-invasive neuroimaging using near-infrared light

    Biol. Psychiatry

    (2002)
  • A.M. Kuncel et al.

    Selection of stimulus parameters for deep brain stimulation

    Clin. Neurophysiol.

    (2004)
  • L. Bareket et al.

    Semiconductor nanorod-carbon nanotube biomimetic films for wire-free photostimulation of blind retinas

    Nano Lett.

    (2014)
  • F. Di Maria et al.

    The evolution of artificial light actuators in living systems: from planar to nanostructured interfaces

    Chem. Soc. Rev.

    (2018)
  • L. Fenno et al.

    The development and application of optogenetics

    Annu. Rev. Neurosci.

    (2011)
  • C. Paviolo et al.

    Nanoparticle-enhanced infrared neural stimulation

    J. Neural Eng.

    (2014)
  • P. Fromherz et al.

    Silicon-neuron junction: capacitive stimulation of an individual neuron on a silicon chip

    Phys. Rev. Lett.

    (1995)
  • Y. Goda et al.

    Photoconductive stimulation of neurons cultured on silicon wafers

    Nat. Protoc.

    (2006)
  • A. Starovoytov et al.

    Light-directed electrical stimulation of neurons cultured on silicon wafers

    J. Neurophysiol.

    (2005)
  • J. Suzurikawa et al.

    Light-addressed stimulation under Ca2+ imaging of cultured neurons

    IEEE Trans. Biomed. Eng.

    (2009)
  • V. Gautam et al.

    Single-pixel, single-layer polymer device as a tricolor sensor with signals mimicking natural photoreceptors

    J. Am. Chem. Soc.

    (2011)
  • D. Ghezzi et al.

    A hybrid bioorganic interface for neuronal photoactivation

    Nat. Commun.

    (2011)
  • M.R. Antognazza et al.

    Characterization of a polymer-based, fully organic prosthesis for implantation into the subretinal space of the rat

    Adv. Healthc. Mater.

    (2016)
  • K. Lugo et al.

    Remote switching of cellular activity and cell signaling using light in conjunction with quantum dots

    Biomed. Opt. Express

    (2012)
  • T.C. Pappas et al.

    Nanoscale engineering of a cellular interface with semiconductor nanoparticle films for photoelectric stimulation of neurons

    Nano Lett.

    (2007)
  • E. Molokanova et al.

    Quantum dots move beyond fluorescence imaging - the unique properties of quantum dots allow them to be optimized for voltage sensing and for light-controlled electrical activation of cells

    Invit. Corp.

    (2008)
  • Cited by (10)

    • Towards optical neuromodulation using nitrogen-doped ultrananocrystalline diamond photoelectrodes

      2022, Surfaces and Interfaces
      Citation Excerpt :

      A capacitive transfer of charge in response to light is more desirable compared to a direct (Faradaic) electron transfer, which is known to cause damage to tissue through the introduction of free radicals [31]. During capacitive charge transfer, there is no direct transfer of charge across the photo-illuminated N-UNCD/electrolyte interface, but instead a redistribution of charged chemical species within the electrolyte [7,36]. The potentiostat indirectly measures this capacitive current by the flow of charge through the counter electrode caused by the photogenerated build-up of charge at the working electrode.

    • Translational considerations for the design of untethered nanomaterials in human neural stimulation

      2021, Brain Stimulation
      Citation Excerpt :

      However, most studies involving these nanomaterials are not focused on the central nervous system (CNS), and have rarely been tested in vivo [56]. Furthermore, novel carbon nanomaterials such as nitrogen-doped ultrananocristalline diamonds have been recently developed and suggested for in vivo use, as they have shown promising preliminary results in vitro for optical neurostimulation [60]. While magnetic fields are able to penetrate deeply into the skull and soft tissue, conventional transcranial approaches such as TMS lack proper spatial resolution, and the power densities required can yield significant off-target effects [23].

    • Enhanced electrochemical capacitance of nitrogen-doped ultrananocrystalline diamond through oxygen treatment

      2021, Applied Surface Science
      Citation Excerpt :

      After deposition, the N-UNCD surface can be terminated with other chemical species to suit specific applications and the desired physical properties. In particular, oxygen on the surface of diamond films has been found to influence their chemical reactivity [8], electrochemical capacitance [9], field emission [10], electrical conductivity [11], and biocompatibility [12]. Oxygen terminated diamond is a hydrophilic material with a widely reported high biocompatibility [12–14], capacitive charge transfer [9], and a large water window [15].

    View all citing articles on Scopus
    View full text