Silicon-based materials have been widely used in biological applications. However, remotely controlled and interconnect-free silicon configurations have been rarely explored, because of limited fundamental understanding of the complex physicochemical processes that occur at interfaces between silicon and biological materials. Here, we describe rational design principles, guided by biology, for establishing intracellular, intercellular and extracellular silicon-based interfaces, where the silicon and the biological targets have matched properties. We focused on light-induced processes at these interfaces, and developed a set of matrices to quantify and differentiate the capacitive, Faradaic and thermal outputs from about 30 different silicon materials in saline. We show that these interfaces are useful for the light-controlled non-genetic modulation of intracellular calcium dynamics, of cytoskeletal structures and transport, of cellular excitability, of neurotransmitter release from brain slices and of brain activity in vivo.
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Viventi, J. et al. Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo. Nat. Neurosci. 14, 1599–1605 (2011).
Tian, B., Cohen-Karni, T., Qing, Q., Duan, X., Xie, P. & Lieber, C. M. Three-dimensional, flexible nanoscale field-effect transistors as localized bioprobes. Science 329, 830–834 (2010).
Liu, J. et al. Syringe-injectable electronics. Nat. Nanotech. 10, 629–636 (2015).
Chiappini, C. et al. Biodegradable silicon nanoneedles delivering nucleic acids intracellularly induce localized in vivo neovascularization. Nat. Mater. 14, 532–539 (2015).
Tian, B. et al. Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. Nat. Mater. 11, 986–994 (2012).
Fang, H. et al. Capacitively coupled arrays of multiplexed flexible silicon transistors for long-term cardiac electrophysiology. Nat. Biomed. Eng. 1, 0038 (2017).
Colicos, M. A., Collins, B. E., Sailor, M. J. & Goda, Y. Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107, 605–616 (2001).
Tee, B. C. et al. A skin-inspired organic digital mechanoreceptor. Science 350, 313–316 (2015).
Khodagholy, D. et al. NeuroGrid: recording action potentials from the surface of the brain. Nat. Neurosci. 18, 310–315 (2015).
Fu, T. M. et al. Stable long-term chronic brain mapping at the single-neuron level. Nat. Methods 13, 875–882 (2016).
Chortos, A., Liu, J. & Bao, Z. Pursuing prosthetic electronic skin. Nat. Mater. 15, 937–950 (2016).
Someya, T., Bao, Z. & Malliaras, G. G. The rise of plastic bioelectronics. Nature 540, 379–385 (2016).
Chiappini, C. et al. Biodegradable nanoneedles for localized delivery of nanoparticles in vivo: exploring the biointerface. ACS Nano 9, 5500–5509 (2015).
Zimmerman, J. F. et al. Free-standing kinked silicon nanowires for probing inter- and intracellular force dynamics. Nano Lett. 15, 5492–5498 (2015).
Chu, B., Burnett, W., Chung, J. W. & Bao, Z. Bring on the bodyNET. Nature 549, 328–330 (2017).
Sakimoto, K. K., Wong, A. B. & Yang, P. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351, 74–77 (2016).
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).
Chen, R., Romero, G., Christiansen, M. G., Mohr, A. & Anikeeva, P. Wireless magnetothermal deep brain stimulation. Science 347, 1477–1480 (2015).
Seo, D. et al. Wireless recording in the peripheral nervous system with ultrasonic neural dust. Neuron 91, 529–539 (2016).
Nadeau, P. et al. Prolonged energy harvesting for ingestible devices. Nat. Biomed. Eng. 1, 0022 (2017).
Jiang, Y. et al. Heterogeneous silicon mesostructures for lipid-supported bioelectric interfaces. Nat. Mater. 15, 1023–1030 (2016).
Grossman, N. et al. Noninvasive deep brain stimulation via temporally interfering electric fields. Cell 169, 1029–1041 (2017).
Dagdeviren, C. et al. Flexible piezoelectric devices for gastrointestinal motility sensing. Nat. Biomed. Eng. 1, 807–817 (2017).
Zimmerman, J. F. et al. Cellular uptake and dynamics of unlabeled freestanding silicon nanowires. Sci. Adv. 2, e1601039 (2016).
Dalby, M. J., Gadegaard, N. & Oreffo, R. O. Harnessing nanotopography and integrin–matrix interactions to influence stem cell fate. Nat. Mater. 13, 558–569 (2014).
Tian, B. et al. Coaxial silicon nanowires as solar cells and nanoelectronic power sources. Nature 449, 885–889 (2007).
Ghezzi, D. et al. A polymer optoelectronic interface restores light sensitivity in blind rat retinas. Nat. Photon. 7, 400–406 (2013).
Walter, M. G. et al. Solar water splitting cells. Chem. Rev. 110, 6446–6473 (2010).
Kang, D. et al. Electrochemical synthesis of photoelectrodes and catalysts for use in solar water splitting. Chem. Rev. 115, 12839–12887 (2015).
Merrill, D. R., Bikson, M. & Jefferys, J. G. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J. Neurosci. Methods 141, 171–198 (2005).
Ziegenfuss, J. S. et al. Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling. Nature 453, 935–939 (2008).
Yoon, J., Park, J., Choi, M., Choi, W. J. & Choi, C. Application of femtosecond-pulsed lasers for direct optical manipulation of biological functions. Ann. Phys. 525, 205–214 (2013).
White, J. A., Blackmore, P. F., Schoenbach, K. H. & Beebe, S. J. Stimulation of capacitative calcium entry in HL-60 cells by nanosecond pulsed electric fields. J. Biol. Chem. 279, 22964–22972 (2004).
Hua, W., Young, E. C., Fleming, M. L. & Gelles, J. Coupling of kinesin steps to ATP hydrolysis. Nature 388, 390–393 (1997).
Stout, C. E., Costantin, J. L., Naus, C. C. & Charles, A. C. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 277, 10482–10488 (2002).
Guthrie, P. B., Knappenberger, J., Segal, M., Bennett, M. V., Charles, A. C. & Kater, S. B. ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520–528 (1999).
Chen, H. X. & Diebold, G. Chemical generation of acoustic waves: a giant photoacoustic effect. Science 270, 963–966 (1995).
Tang-Schomer, M. D., Patel, A. R., Baas, P. W. & Smith, D. H. Mechanical breaking of microtubules in axons during dynamic stretch injury underlies delayed elasticity, microtubule disassembly, and axon degeneration. FASEB J. 24, 1401–1410 (2010).
Maya-Vetencourt, J. F. et al. A fully organic retinal prosthesis restores vision in a rat model of degenerative blindness. Nat. Mater. 16, 681–689 (2017).
Ghezzi, D. et al. A hybrid bioorganic interface for neuronal photoactivation. Nat. Commun. 2, 166 (2011).
Lorach, H. et al. Photovoltaic restoration of sight with high visual acuity. Nat. Med. 21, 476–482 (2015).
Katz, L. C. & Dalva, M. B. Scanning laser photostimulation: a new approach for analyzing brain circuits. J. Neurosci. Methods 54, 205–218 (1994).
Yamawaki, N., Suter, B. A., Wickersham, I. R. & Shepherd, G. M. Combining optogenetics and electrophysiology to analyze projection neuron circuits. Cold Spring Harb. Protoc. https://doi.org/10.1101/pdb.prot090084 (2016).
Paralikar, K. J., Rao, C. R. & Clement, R. S. New approaches to eliminating common-noise artifacts in recordings from intracortical microelectrode arrays: inter-electrode correlation and virtual referencing. J. Neurosci. Methods 181, 27–35 (2009).
Veerabhadrappa, R. et al. Unified selective sorting approach to analyse multi-electrode extracellular data. Sci. Rep. 6, 28533 (2016).
Rossant, C. et al. Spike sorting for large, dense electrode arrays. Nat. Neurosci. 19, 634–641 (2016).
Yamawaki, N., Borges, K., Suter, B. A., Harris, K. D. & Shepherd, G. M. A genuine layer 4 in motor cortex with prototypical synaptic circuit connectivity. Elife 3, e05422 (2014).
Li, X., Yamawaki, N., Barrett, J. M., Kording, K. P. & Shepherd, G. M. G. Corticocortical signaling drives activity in a downstream area rapidly and scalably. Preprint at https://doi.org/10.1101/154914 (2017).
Tennant, K. A. et al. The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb. Cortex 21, 865–876 (2011).
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).
Dai, J., Brooks, D. I. & Sheinberg, D. L. Optogenetic and electrical microstimulation systematically bias visuospatial choice in primates. Curr. Biol. 24, 63–69 (2014).
Stauffer, W. R. et al. Dopamine neuron-specific optogenetic stimulation in rhesus macaques. Cell 166, 1564–1571 (2016).
Chen, R., Canales, A. & Anikeeva, P. Neural recording and modulation technologies. Nat. Rev. Mater. 2, 16093 (2017).
Voyles, P. M., Grazul, J. L. & Muller, D. A. Imaging individual atoms inside crystals with ADF-STEM. Ultramicroscopy 96, 251–273 (2003).
Voyles, P. M., Muller, D. A., Grazul, J. L., Citrin, P. H. & Gossmann, H. J. Atomic-scale imaging of individual dopant atoms and clusters in highly n-type bulk Si. Nature 416, 826–829 (2002).
Suter, B. A. et al. Ephus: multipurpose data acquisition software for neuroscience experiments. Front. Neural Circuits 4, 100 (2010).
Yao, J., Liu, B. & Qin, F. Rapid temperature jump by infrared diode laser irradiation for patch-clamp studies. Biophys. J. 96, 3611–3619 (2009).
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 Searle Scholars Foundation and the National Institutes of Health (NIH NS101488, and NS061963). This work made use of the Japan Electron Optics Laboratory (JEOL) JEM-ARM200CF and JEOL JEM-3010 TEM in the Electron Microscopy Service of the Research Resources Center at the University of Illinois at Chicago (UIC). The acquisition of the UIC JEOL JEM-ARM200CF was supported by a MRI-R2 grant from the National Science Foundation (DMR-0959470). The animal imaging work conducted at the Integrated Small Animal Imaging Research Resource (iSAIRR) at the University of Chicago was supported in part by funding provided by the Virginia and D. K. Ludwig Fund for Cancer Research via the Imaging Research Institute in the Biological Sciences Division, by the University of Chicago Comprehensive Cancer Center including an NIH grant P30 CA14599, and by the Department of Radiology. Part of the schematic in Fig. 5c was generated from a three-dimensional anatomy software purchased from https://biosphera.org. The authors thank L. Yu, V. Sharapov, S. Patel, Y. Chen, Q. Guo and J. Jureller for providing technical support.
The authors declare no competing interests.
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Supplementary figures, tables, video captions and references.
Left forelimb movement triggered by the photostimulation of a Si mesh (~4 mW for 50 ms).
Left forelimb movement triggered by the photostimulation of a Si mesh (~5 mW for 50 ms).
Right forelimb movement triggered by the photostimulation of a Si mesh (~5 mW for 50 ms).
Right forelimb movement triggered by the photostimulation of a Si mesh (~5 mW for 100 ms).
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Jiang, Y., Li, X., Liu, B. et al. Rational design of silicon structures for optically controlled multiscale biointerfaces. Nat Biomed Eng 2, 508–521 (2018). https://doi.org/10.1038/s41551-018-0230-1
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