Photoelectrochemical modulation of neuronal activity with free-standing coaxial silicon nanowires

Abstract

Optical methods for modulating cellular behaviour are promising for both fundamental and clinical applications. However, most available methods are either mechanically invasive, require genetic manipulation of target cells or cannot provide subcellular specificity. Here, we address all these issues by showing optical neuromodulation with free-standing coaxial p-type/intrinsic/n-type silicon nanowires. We reveal the presence of atomic gold on the nanowire surfaces, likely due to gold diffusion during the material growth. To evaluate how surface gold impacts the photoelectrochemical properties of single nanowires, we used modified quartz pipettes from a patch clamp and recorded sustained cathodic photocurrents from single nanowires. We show that these currents can elicit action potentials in primary rat dorsal root ganglion neurons through a primarily atomic gold-enhanced photoelectrochemical process.

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Fig. 1: XPS and APT reveal the presence of atomic Au on coaxial NW surfaces.
Fig. 2: Single NW recordings reveal that coaxial SiNWs are photoelectrochemical current sources.
Fig. 3: Basic SiNW-based neural interfaces can be formed.
Fig. 4: Photocurrent generated by coaxial NWs can be harnessed to elicit APs in primary rat DRG neurons.
Fig. 5: Mechanism of coaxial NW photocurrent generation and neuronal modulation is primarily photoelectrochemical, aided by surface atomic Au.

References

  1. 1.

    Famm, K., Litt, B., Tracey, K. J., Boyden, E. S. & Slaoui, M. A jump-start for electroceuticals. Nature 496, 159–161 (2013).

    CAS  Article  Google Scholar 

  2. 2.

    Vetter, R. J., Williams, J. C., Hetke, J. F., Nunamaker, E. A. & Kipke, D. R. Chronic neural recording using silicon-substrate microelectrode arrays implanted in cerebral cortex. IEEE Trans. Biomed. Eng. 51, 896–904 (2004).

    Article  Google Scholar 

  3. 3.

    Zhou, W., Dai, X. C. & Lieber, C. M. Advances in nanowire bioelectronics. Rep. Prog. Phys. 80, 016701 (2017).

    Article  Google Scholar 

  4. 4.

    Ghezzi, D. et al. A hybrid bioorganic interface for neuronal photoactivation. Nat. Commun. 2, 166 (2011).

    Article  Google Scholar 

  5. 5.

    Ghezzi, D. et al. A polymer optoelectronic interface restores light sensitivity in blind rat retinas. Nat. Photon. 7, 400–406 (2013).

    CAS  Article  Google Scholar 

  6. 6.

    Mathieson, K. et al. Photovoltaic retinal prosthesis with high pixel density. Nat. Photon. 6, 391–397 (2012).

  7. 7.

    Carvalho-de-Souza, J. L. et al. Photosensitivity of neurons enabled by cell-targeted gold nanoparticles. Neuron 86, 207–217 (2015).

    CAS  Article  Google Scholar 

  8. 8.

    Jiang, Y. W. et al. Heterogeneous silicon rnesostructures for lipid-supported bioelectric interfaces. Nat. Mater. 15, 1023–1030 (2016).

    CAS  Article  Google Scholar 

  9. 9.

    Packer, A. M., Roska, B. & Hausser, M. Targeting neurons and photons for optogenetics. Nat. Neurosci. 16, 805–815 (2013).

    CAS  Article  Google Scholar 

  10. 10.

    Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263–1268 (2005).

    CAS  Article  Google Scholar 

  11. 11.

    Zimmerman, J., Parameswaran, R. & Tian, B. Z. Nanoscale semiconductor devices as new biomaterials. Biomater. Sci. 2, 619–626 (2014).

    CAS  Article  Google Scholar 

  12. 12.

    Rogers, J. A., Someya, T. & Huang, Y. G. Materials and mechanics for stretchable electronics. Science 327, 1603–1607 (2010).

    CAS  Article  Google Scholar 

  13. 13.

    Hwang, S. W. et al. A physically transient form of silicon electronics. Science 337, 1640–1644 (2012).

    CAS  Article  Google Scholar 

  14. 14.

    Straub, B., Meyer, E. & Fromherz, P. Recombinant maxi-K channels on transistor, a prototype of iono-electronic interfacing. Nat. Biotechnol. 19, 121–124 (2001).

    CAS  Article  Google Scholar 

  15. 15.

    Chiappini, C. et al. Biodegradable silicon nanoneedles delivering nucleic acids intracellularly induce localized in vivo neovascularization. Nat. Mater. 14, 532–539 (2015).

    CAS  Article  Google Scholar 

  16. 16.

    Priolo, F., Gregorkiewicz, T., Galli, M. & Krauss, T. F. Silicon nanostructures for photonics and photovoltaics. Nat. Nanotech. 9, 19–32 (2014).

  17. 17.

    Xie, P., Xiong, Q. H., Fang, Y., Qing, Q. & Lieber, C. M. Local electrical potential detection of DNA by nanowire-nanopore sensors. Nat. Nanotech. 7, 119–125 (2012).

    CAS  Article  Google Scholar 

  18. 18.

    Yan, R. et al. Nanowire-based single-cell endoscopy. Nat. Nanotech. 7, 191–196 (2012).

  19. 19.

    Zimmerman, J. F. et al. Cellular uptake and dynamics of unlabeled freestanding silicon nanowires. Sci. Adv. 2, e1601039 (2016).

  20. 20.

    Zhang, A. Q. & Lieber, C. M. Nano-bioelectronics. Chem. Rev. 116, 215–257 (2016).

    CAS  Article  Google Scholar 

  21. 21.

    Tian, B. Z. et al. Coaxial silicon nanowires as solar cells and nanoelectronic power sources. Nature 449, 885–888 (2007).

    CAS  Article  Google Scholar 

  22. 22.

    Su, Y. D. et al. Single-nanowire photoelectrochemistry. Nat. Nanotech. 11, 609–612 (2016).

    CAS  Article  Google Scholar 

  23. 23.

    Hannon, J. B., Kodambaka, S., Ross, F. M. & Tromp, R. M. The influence of the surface migration of gold on the growth of silicon nanowires. Nature 440, 69–71 (2006).

    CAS  Article  Google Scholar 

  24. 24.

    Luo, Z. Q. et al. Atomic gold-enabled three-dimensional lithography for silicon mesostructures. Science 348, 1451–1455 (2015).

    CAS  Article  Google Scholar 

  25. 25.

    Seibt, M. et al. Gettering in silicon photovoltaics: current state and future perspectives. Phys. Stat. Solidi A Appl. Mater. Sci. 203, 696–713 (2006).

  26. 26.

    Yuan, G. B. et al. Understanding the origin of the low performance of chemically grown silicon nanowires for solar energy conversion. Angew. Chem. Int. Ed. 50, 2334–2338 (2011).

    CAS  Article  Google Scholar 

  27. 27.

    Kim, S. K. et al. Tuning light absorption in core/shell silicon nanowire photovoltaic devices through morphological design. Nano Lett. 12, 4971–4976 (2012).

    CAS  Article  Google Scholar 

  28. 28.

    Garnett, E. C. et al. Dopant profiling and surface analysis of silicon nanowires using capacitance–voltage measurements. Nat. Nanotech. 4, 311–314 (2009).

    CAS  Article  Google Scholar 

  29. 29.

    Liu, Z. et al. Anomalous high capacitance in a coaxial single nanowire capacitor. Nat. Commun. 3, 879 (2012).

    Article  Google Scholar 

  30. 30.

    Vogel, E. M. Technology and metrology of new electronic materials and devices. Nat. Nanotech. 2, 25–32 (2007).

    CAS  Article  Google Scholar 

  31. 31.

    Mogyoros, I., Kiernan, M. C., Burke, D. & Bostock, H. Strength-duration properties of sensory and motor axons in amyotrophic lateral sclerosis. Brain 121, 851–859 (1998).

    Article  Google Scholar 

  32. 32.

    Walter, M. G. et al. Solar water splitting cells. Chem. Rev. 110, 6446–6473 (2010).

    CAS  Article  Google Scholar 

  33. 33.

    Warren, E. L., McKone, J. R., Atwater, H. A., Graya, H. B. & Lewis, N. S. Hydrogen-evolution characteristics of Ni-Mo-coated, radial junction, n+p-silicon microwire array photocathodes. Energy Environ. Sci. 5, 9653–9661 (2012).

  34. 34.

    Sachsenhauser, M., Sharp, I. D., Stutzmann, M. & Garrido, J. A. Surface state mediated electron transfer across the n-type SiC/electrolyte interface. J. Phys. Chem. C 120, 6524–6533 (2016).

  35. 35.

    Lee, J. H., Zhang, A. Q., You, S. S. & Lieber, C. M. Spontaneous internalization of cell penetrating peptide-modified nanowires into primary neurons. Nano Lett. 16, 1509–1513 (2016).

    CAS  Article  Google Scholar 

  36. 36.

    Liu, C., Colon, B. C., Ziesack, M., Silver, P. A. & Nocera, D. G. Water splitting–biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis. Science 352, 1210–1213 (2016).

    CAS  Article  Google Scholar 

  37. 37.

    Sakimoto, K. K., Wong, A. B. & Yang, P. D. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351, 74–77 (2016).

    CAS  Article  Google Scholar 

  38. 38.

    Silva, G. A. Neuroscience nanotechnology: progress, opportunities and challenges. Nat. Rev. Neurosci. 7, 65–74 (2006).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank F. Shi at the University of Illinois Chicago for her help in collecting the EDS data. This work is supported by the Air Force Office of Scientific Research (AFOSR FA9550-14-1-0175, FA9550-15-1-0285), the National Science Foundation (NSF CAREER, DMR-1254637; NSF MRSEC, DMR 1420709), the Alfred P. Sloan Foundation Fellowship (FG-2016-6805), the Searle Scholars Foundation, the National Institute of Health (NIH GM030376, NIH F30AI138156, and NS101488), MSTP Training Grant (T32GM007281) and the Paul and Daisy Soros Foundation.

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R.P. grew SiNWs for all experiments and performed all neuron electrophysiology experiments. R.P. and M.J.B. analysed neuron electrophysiology data. Y.J. performed and analysed STEM data. Y.J., J.Y. and R.P. prepared samples for, performed and analysed APT experiments. K.K. performed and analysed XPS experiments. R.P. and A.P. prepared samples for and performed SEM on neuron/SiNW samples. R.P. and M.J.B. performed and analysed LIVE/DEAD and fluorescence microscopy experiments. J.L.C.-d.-S. and R.P. set up equipment for all neuron electrophysiology experiments, temperature recordings and photocurrent recordings. R.P., J.F.Z. and J.L.C.-d.-S. developed the single NW photocurrent recording method. R.P. performed and analysed all photocurrent and temperature recordings. E.J.A. provided support and input on all experiments. B.T. and F.B. directed the research. R.P. and B.T. co-wrote the paper. All authors read and commented on the manuscript.

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Correspondence to Francisco Bezanilla or Bozhi Tian.

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Supplementary Table 1, Supplementary Figures 1–11.

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Parameswaran, R., Carvalho-de-Souza, J.L., Jiang, Y. et al. Photoelectrochemical modulation of neuronal activity with free-standing coaxial silicon nanowires. Nature Nanotech 13, 260–266 (2018). https://doi.org/10.1038/s41565-017-0041-7

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