Advertisement

Nano Research

, Volume 11, Issue 10, pp 5065–5106 | Cite as

Nano functional neural interfaces

  • Yongchen Wang
  • Hanlin Zhu
  • Huiran Yang
  • Aaron D. Argall
  • Lan Luan
  • Chong XieEmail author
  • Liang GuoEmail author
Review Article

Abstract

Engineered functional neural interfaces (fNIs) serve as essential abiotic–biotic transducers between an engineered system and the nervous system. They convert external physical stimuli to cellular signals in stimulation mode or read out biological processes in recording mode. Information can be exchanged using electricity, light, magnetic fields, mechanical forces, heat, or chemical signals. fNIs have found applications for studying processes in neural circuits from cell cultures to organs to whole organisms. fNI-facilitated signal transduction schemes, coupled with easily manipulable and observable external physical signals, have attracted considerable attention in recent years. This enticing field is rapidly evolving toward miniaturization and biomimicry to achieve long-term interface stability with great signal transduction efficiency. Not only has a new generation of neuroelectrodes been invented, but the use of advanced fNIs that explore other physical modalities of neuromodulation and recording has begun to increase. This review covers these exciting developments and applications of fNIs that rely on nanoelectrodes, nanotransducers, or bionanotransducers to establish an interface with the nervous system. These nano fNIs are promising in offering a high spatial resolution, high target specificity, and high communication bandwidth by allowing for a high density and count of signal channels with minimum material volume and area to dramatically improve the chronic integration of the fNI to the target neural tissue. Such demanding advances in nano fNIs will greatly facilitate new opportunities not only for studying basic neuroscience but also for diagnosing and treating various neurological diseases.

Keywords

neural interface neurotechnology nanoelectrode nanomaterial neural recording neural stimulation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

L. G. is supported by The Defense Advanced Research Projects Agency (No. D17AP00031) of the USA. The views, opinions, and/or findings contained in this article are those of the author and should not be interpreted as representing the official views or policies, either expressed or implied, of the Defense Advanced Research Projects Agency or the Department of Defense.

References

  1. [1]
    Fenno, L.; Yizhar, O.; Deisseroth, K. The development and application of optogenetics. Ann. Rev. Neurosci. 2011, 34, 389–412.Google Scholar
  2. [2]
    Guo, L. The pursuit of chronically reliable neural interfaces: A materials perspective. Front. Neurosci. 2016, 10, 599.Google Scholar
  3. [3]
    Marin, C.; Fernández, E. Biocompatibility of intracortical microelectrodes: Current status and future prospects. Front. Neuroeng. 2010, 3, 8.Google Scholar
  4. [4]
    Polikov, V. S.; Tresco, P. A.; Reichert, W. M. Response of brain tissue to chronically implanted neural electrodes. J. Neurosci. Methods 2005, 148, 1–18.Google Scholar
  5. [5]
    Barrese, J. C.; Rao, N.; Paroo, K.; Triebwasser, C.; Vargas–Irwin, C.; Franquemont, L.; Donoghue, J. P. Failure mode analysis of silicon–based intracortical microelectrode arrays in non–human primates. J. Neural Eng. 2013, 10, 066014.Google Scholar
  6. [6]
    Kozai, T. D. Y.; Catt, K.; Li, X.; Gugel, Z. V.; Olafsson, V. T.; Vazquez, A. L.; Cui, X. T. Mechanical failure modes of chronically implanted planar silicon–based neural probes for laminar recording. Biomaterials 2015, 37, 25–39.Google Scholar
  7. [7]
    McConnell, G. C.; Rees, H. D.; Levey, A. I.; Gutekunst, C.–A.; Gross, R. E.; Bellamkonda, R. V. Implanted neural electrodes cause chronic, local inflammation that is correlated with local neurodegeneration. J. Neural Eng. 2009, 6, 056003.Google Scholar
  8. [8]
    Kozai, T. D. Y.; Langhals, N. B.; Patel, P. R.; Deng, X. P.; Zhang, H. N.; Smith, K. L.; Lahann, J.; Kotov, N. A.; Kipke, D. R. Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat. Mater. 2012, 11, 1065–1073.Google Scholar
  9. [9]
    Xie, C.; Liu, J.; Fu, T. M.; Dai, X. C.; Zhou, W.; Lieber, C. M. Three–dimensional macroporous nanoelectronic networks as minimally invasive brain probes. Nat. Mater. 2015, 14, 1286–1292.Google Scholar
  10. [10]
    Luan, L.; Wei, X. L.; Zhao, Z. T.; Siegel, J. J.; Potnis, O.; Tuppen, C. A.; Lin, S. Q.; Kazmi, S.; Fowler, R. A.; Holloway, S. et al. Ultraflexible nanoelectronic probes form reliable, glial scar–free neural integration. Sci. Adv. 2017, 3, e1601966.Google Scholar
  11. [11]
    Huang, H.; Delikanli, S.; Zeng, H.; Ferkey, D. M.; Pralle, A. Remote control of ion channels and neurons through magnetic–field heating of nanoparticles. Nat. Nanotechnol. 2010, 5, 602–606.Google Scholar
  12. [12]
    McCreery, D. B.; Agnew, W. F.; Yuen, T. G. H.; Bullara, L. Charge–density and charge per phase as cofactors in neural injury induced by electrical–stimulation. IEEE Trans. Biomed. Eng. 1990, 37, 996–1001.Google Scholar
  13. [13]
    Kim, J. H.; Manuelidis, E. E.; Glen, W. W.; Kaneyuki, T. Diaphragm pacing: Histopathological changes in the phrenic nerve following long–term electrical stimulation. J. Thorac. Cardiovasc. Surg. 1976, 72, 602–608.Google Scholar
  14. [14]
    Kotov, N. A.; Winter, J. O.; Clements, I. P.; Jan, E.; Timko, B. P.; Campidelli, S.; Pathak, S.; Mazzatenta, A.; Lieber, C. M.; Prato, M. et al. Nanomaterials for neural interfaces. Adv. Mater. 2009, 21, 3970–4004.Google Scholar
  15. [15]
    Wang, Y. C.; Guo, L. Nanomaterial–enabled neural stimulation. Front. Neurosci. 2016, 10, 69.Google Scholar
  16. [16]
    Young, A. T.; Cornwell, N.; Daniele, M. A. Neuro–nano interfaces: Utilizing nano–coatings and nanoparticles to enable next–generation electrophysiological recording, neural stimulation, and biochemical modulation. Adv. Funct. Mater. 2017, 28, 1700239.Google Scholar
  17. [17]
    Krack, P.; Batir, A.; Van Blercom, N.; Chabardes, S.; Fraix, V.; Ardouin, C.; Koudsie, A.; Limousin, P. D.; Benazzouz, A.; LeBas, J. F. et al. Five–year follow–up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N. Engl. J. Med. 2003, 349, 1925–1934.Google Scholar
  18. [18]
    Boon, P.; Raedt, R.; De Herdt, V.; Wyckhuys, T.; Vonck, K. Electrical stimulation for the treatment of epilepsy. Neurotherapeutics 2009, 6, 218–227.Google Scholar
  19. [19]
    Burgess, N. The 2014 Nobel Prize in physiology or medicine: A spatial model for cognitive neuroscience. Neuron 2014, 84, 1120–1125.Google Scholar
  20. [20]
    Kim, T. I.; McCall, J. G.; Jung, Y. H.; Huang, X.; Siuda, E. R.; Li, Y.; Song, J.; Song, Y. M.; Pao, H. A.; Kim, R. H. et al. Injectable, cellular–scale optoelectronics with applications for wireless optogenetics. Science 2013, 340, 211–216.Google Scholar
  21. [21]
    Kozai, T. D. Y.; Du, Z. H.; Gugel, Z. V.; Smith, M. A.; Chase, S. M.; Bodily, L. M.; Caparosa, E. M.; Friedlander, R. M.; Cui, X. T. Comprehensive chronic laminar single–unit, multi–unit, and local field potential recording performance with planar single shank electrode arrays. J. Neurosci. Methods 2015, 242, 15–40.Google Scholar
  22. [22]
    Fraser, G. W.; Schwartz, A. B. Recording from the same neurons chronically in motor cortex. J. Neurophysiol. 2012, 107, 1970–1978.Google Scholar
  23. [23]
    Perge, J. A.; Homer, M. L.; Malik, W. Q.; Cash, S.; Eskandar, E.; Friehs, G.; Donoghue, J. P.; Hochberg, L. R. Intra–day signal instabilities affect decoding performance in an intracortical neural interface system. J. Neural. Eng. 2013, 10, 036004.Google Scholar
  24. [24]
    Gilletti, A.; Muthuswamy, J. Brain micromotion around implants in the rodent somatosensory cortex. J. Neural. Eng. 2006, 3, 189–195.Google Scholar
  25. [25]
    Prasad, A.; Xue, Q. S.; Dieme, R.; Sankar, V.; Mayrand, R. C.; Nishida, T.; Streit, W. J.; Sanchez, J. C. Abiotic–biotic characterization of Pt/Ir microelectrode arrays in chronic implants. Front. Neuroeng. 2014, 7, 2.Google Scholar
  26. [26]
    Prasad, A.; Xue, Q. S.; Sankar, V.; Nishida, T.; Shaw, G.; Streit, W. J.; Sanchez, J. C. Comprehensive characterization and failure modes of tungsten microwire arrays in chronic neural implants. J. Neural. Eng. 2012, 9, 056015.Google Scholar
  27. [27]
    Gilgunn, P. J.; Ong, X. C.; Flesher, S. N.; Schwartz, A. B.; Gaunt, R. A. Structural analysis of explanted microelectrode arrays. In Proceedings of the 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER), San Diego, CA, USA, 2013, pp 719–722.Google Scholar
  28. [28]
    Patel, P. R.; Na, K.; Zhang, H. N; Kozai, T. D. Y.; Kotov, N. A.; Yoon, E.; Chestek, C. A. Insertion of linear 8.4 μm diameter 16 channel carbon fiber electrode arrays for single unit recordings. J. Neural Eng. 2015, 12, 046009.Google Scholar
  29. [29]
    Rousche, P. J.; Normann, R. A. Chronic recording capability of the Utah Intracortical Electrode Array in cat sensory cortex. J. Neurosci. Methods 1998, 82, 1–15.Google Scholar
  30. [30]
    Williams, J. C.; Rennaker, R. L.; Kipke, D. R. Long–term neural recording characteristics of wire microelectrode arrays implanted in cerebral cortex. Brain Res. Protoc. 1999, 4, 303–313.Google Scholar
  31. [31]
    Kipke, D. R.; Vetter, R. J.; Williams, J. C.; Hetke, J. F. Silicon–substrate intracortical microelectrode arrays for long–term recording of neuronal spike activity in cerebral cortex. IEEE Trans. Neural Syst. Rehabil. Eng. 2003, 11, 151–155.Google Scholar
  32. [32]
    Simeral, J. D.; Kim, S. P.; Black, M. J.; Donoghue, J. P.; Hochberg, L. R. Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array. J. Neural Eng. 2011, 8, 025027.Google Scholar
  33. [33]
    Sakmann, B.; Neher, E. Single–Channel Recording, 2nd ed.; Springer: New York, NY, USA, 2009.Google Scholar
  34. [34]
    Souslova, V.; Cesare, P.; Ding, Y. N.; Akopian, A. N.; Stanfa, L.; Suzuki, R.; Carpenter, K.; Dickenson, A.; Boyce, S.; Hill, R. et al. Warm–coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature 2000, 407, 1015–1017.Google Scholar
  35. [35]
    Lee, J.; Ishihara, A.; Oxford, G.; Johnson, B.; Jacobson, K. Regulation of cell movement is mediated by stretchactivated calcium channels. Nature 1999, 400, 382–386.Google Scholar
  36. [36]
    Thomas, C. A., Jr.; Springer, P. A.; Loeb, G. E.; Berwald–Netter, Y.; Okun, L. M. A miniature microelectrode array to monitor the bioelectric activity of cultured cells. Exp. Cell Res. 1972, 74, 61–66.Google Scholar
  37. [37]
    Connolly, P.; Clark, P.; Curtis, A. S.; Dow, J. A. T.; Wilkinson, C. D. An extracellular microelectrode array for monitoring electrogenic cells in culture. Biosens. Bioelectron. 1990, 5, 223–234.Google Scholar
  38. [38]
    Pine, J. Recording action potentials from cultured neurons with extracellular microcircuit electrodes. J. Neurosci. Methods 1980, 2, 19–31.Google Scholar
  39. [39]
    Hai, A.; Spira, M. E. On–chip electroporation, membrane repair dynamics and transient in–cell recordings by arrays of gold mushroom–shaped microelectrodes. Lab Chip 2012, 12, 2865–2873.Google Scholar
  40. [40]
    Xie, C.; Lin, Z. L.; Hanson, L.; Cui, Y.; Cui, B. X. Intracellular recording of action potentials by nanopillar electroporation. Nat. Nanotechnol. 2012, 7, 185–190.Google Scholar
  41. [41]
    Xie, C.; Hanson, L.; Xie, W. J.; Lin, Z. L.; Cui, B. X.; Cui, Y. Noninvasive neuron pinning with nanopillar arrays. Nano Lett. 2010, 10, 4020–4024.Google Scholar
  42. [42]
    Lin, Z. C.; Xie, C.; Osakada, Y.; Cui, Y.; Cui, B. X. Iridium oxide nanotube electrodes for sensitive and prolonged intracellular measurement of action potentials. Nat. Commun. 2014, 5, 3206.Google Scholar
  43. [43]
    Robinson, J. T.; Jorgolli, M.; Shalek, A. K.; Yoon, M.–H.; Gertner, R. S.; Park, H. Vertical nanowire electrode arrays as a scalable platform for intracellular interfacing to neuronal circuits. Nat. Nanotechnol. 2012, 7, 180–184.Google Scholar
  44. [44]
    Abbott, J.; Ye, T. Y.; Qin, L.; Jorgolli, M.; Gertner, R. S.; Ham, D.; Park, H. CMOS nanoelectrode array for allelectrical intracellular electrophysiological imaging. Nat. Nanotechnol. 2017, 12, 460–466.Google Scholar
  45. [45]
    Liu, R.; Chen, R. J.; Elthakeb, A. T.; Lee, S. H.; Hinckley, S.; Khraiche, M. L.; Scott, J.; Pre, D.; Hwang, Y.; Tanaka, A. et al. High density individually addressable nanowire arrays record intracellular activity from primary rodent and human stem cell derived neurons. Nano Lett. 2017, 17, 2757–2764.Google Scholar
  46. [46]
    Tian, B. Z.; Cohen–Karni, T.; Qing, Q.; Duan, X. J.; Xie, P.; Lieber, C. M. Three–dimensional, flexible nanoscale fieldeffect transistors as localized bioprobes. Science 2010, 329, 830–834.Google Scholar
  47. [47]
    Qing, Q.; Jiang, Z.; Xu, L.; Gao, R. X.; Mai, L. Q.; Lieber, C. M. Free–standing kinked nanowire transistor probes for targeted intracellular recording in three dimensions. Nat. Nanotechnol. 2014, 9, 142–147.Google Scholar
  48. [48]
    Duan, X. J.; Gao, R. X.; Xie, P.; Cohen–Karni, T.; Qing, Q.; Choe, H. S.; Tian, B. Z.; Jiang, X. C.; Lieber, C. M. Intracellular recordings of action potentials by an extracellular nanoscale field–effect transistor. Nat. Nanotechnol. 2012, 7, 174–179.Google Scholar
  49. [49]
    Fu, T.–M.; Duan, X. J.; Jiang, Z.; Dai, X. C.; Xie, P.; Cheng, Z. G.; Lieber, C. M. Sub–10–nm intracellular bioelectronic probes from nanowire–nanotube heterostructures. Proc. Natl. Acad. Sci. USA 2014, 111, 1259–1264.Google Scholar
  50. [50]
    Jayant, K.; Hirtz, J. J.; Plante, I. J.–L.; Tsai, D. M.; de Boer, W. D. A. M.; Semonche, A.; Peterka, D. S.; Owen, J. S.; Sahin, O.; Shepard, K. L. et al. Targeted intracellular voltage recordings from dendritic spines using quantum–dot–coated nanopipettes. Nat. Nanotechnol. 2017, 12, 335–342.Google Scholar
  51. [51]
    Kim, R.; Nam, Y. Electrochemical layer–by–layer approach to fabricate mechanically stable platinum black microelectrodes using a mussel–inspired polydopamine adhesive. J. Neural Eng. 2015, 12, 026010.Google Scholar
  52. [52]
    Li, M. Z.; Zhou, Q.; Duan, Y. Y. Nanostructured porous platinum electrodes for the development of low–cost fully implantable cortical electrical stimulator. Sensor. Actuat. B: Chem. 2015, 221, 179–186.Google Scholar
  53. [53]
    Weremfo, A.; Carter, P.; Hibbert, D. B.; Zhao, C. Investigating the interfacial properties of electrochemically roughened platinum electrodes for neural stimulation. Langmuir 2015, 31, 2593–2599.Google Scholar
  54. [54]
    Park, S.; Song, Y. J.; Boo, H.; Chung, T. D. Nanoporous Pt microelectrode for neural stimulation and recording: In vitro characterization. J. Phys. Chem. C 2010, 114, 8721–8726.Google Scholar
  55. [55]
    Lee, Y. J.; Lee, S. J.; Yoon, H. S.; Park, J. Y. A bulk micromachined silicon neural probe with nanoporous platinum electrode for low impedance recording. In SENSORS, 2013 IEEE, Baltimore, MD, USA, 2013, pp 1–4.Google Scholar
  56. [56]
    Chung, T.; Wang, J. Q.; Wang, J.; Cao, B.; Li, Y.; Pang, S. W. Electrode modifications to lower electrode impedance and improve neural signal recording sensitivity. J. Neural Eng. 2015, 12, 056018.Google Scholar
  57. [57]
    Chen, Y.–C.; Hsu, H.–L.; Lee, Y.–T.; Su, H.–C.; Yen, S.–J.; Chen, C.–H.; Hsu, W.–L.; Yew, T.–R.; Yeh, S.–R.; Yao, D.–J. et al. An active, flexible carbon nanotube microelectrode array for recording electrocorticograms. J. Neural Eng. 2011, 8, 034001.Google Scholar
  58. [58]
    Kim, G. H.; Kim, K.; Nam, H.; Shin, K.; Choi, W.; Shin, J. H.; Lim, G. CNT–Au nanocomposite deposition on gold microelectrodes for improved neural recordings. Sensor. Actuat. B: Chem. 2017, 252, 152–158.Google Scholar
  59. [59]
    Kim, J.–H.; Kang, G.; Nam, Y.; Choi, Y.–K. Surfacemodified microelectrode array with flake nanostructure for neural recording and stimulation. Nanotechnology 2010, 21, 085303.Google Scholar
  60. [60]
    Kim, Y. H.; Kim, G. H.; Kim, A. Y.; Han, Y. H.; Chung, M.–A.; Jung, S.–D. In vitro extracellular recording and stimulation performance of nanoporous gold–modified multielectrode arrays. J. Neural Eng. 2015, 12, 066029.Google Scholar
  61. [61]
    Brüggemann, D.; Wolfrum, B.; Maybeck, V.; Mourzina, Y.; Jansen, M.; Offenhäusser, A. Nanostructured gold microelectrodes for extracellular recording from electrogenic cells. Nanotechnology 2011, 22, 265104.Google Scholar
  62. [62]
    Zhou, H. B.; Li, G.; Sun, X. N.; Zhu, Z. H.; Jin, Q. H.; Zhao, J. L.; Ren, Q. S. Integration of Au nanorods with flexible thin–film microelectrode arrays for improved neural interfaces. J. Microelectromech. Syst. 2009, 18, 88–96.Google Scholar
  63. [63]
    Zhao, Z. Y.; Gong, R. X.; Zheng, L.; Wang, J. In vivo neural recording and electrochemical performance of microelectrode arrays modified by rough–surfaced AuPt alloy nanoparticles with nanoporosity. Sensors 2016, 16, 1851.Google Scholar
  64. [64]
    Kim, Y. H.; Kim, G. H.; Kim, M. S.; Jung, S.–D. Iridium oxide–electrodeposited nanoporous gold multielectrode array with enhanced stimulus efficacy. Nano Lett. 2016, 16, 7163–7168.Google Scholar
  65. [65]
    Zeng, Q.; Xia, K.; Sun, B.; Yin, Y. L.; Wu, T. Z.; Humayun, M. S. Electrodeposited iridium oxide on platinum nanocones for improving neural stimulation microelectrodes. Electrochim. Acta 2017, 237, 152–159.Google Scholar
  66. [66]
    Jan, E.; Hendricks, J. L.; Husaini, V.; Richardson–Burns, S. M.; Sereno, A.; Martin, D. C.; Kotov, N. A. Layered carbon nanotube–polyelectrolyte electrodes outperform traditional neural interface materials. Nano Lett. 2009, 9, 4012–4018.Google Scholar
  67. [67]
    Deng, M.; Yang, X.; Silke, M.; Qiu, W. M.; Xu, M. S.; Borghs, G.; Chen, H. Z. Electrochemical deposition of polypyrrole/graphene oxide composite on microelectrodes towards tuning the electrochemical properties of neural probes. Sensor. Actuat. B: Chem. 2011, 158, 176–184.Google Scholar
  68. [68]
    Luo, X. L.; Weaver, C. L.; Tan, S. S.; Cui, X. T. Pure graphene oxide doped conducting polymer nanocomposite for bio–interfacing. J. Mater. Chem. B 2013, 1, 1340–1348.Google Scholar
  69. [69]
    Weaver, C. L.; Li, H.; Luo, X.; Cui, X. T. A graphene oxide/conducting polymer nanocomposite for electrochemical dopamine detection: Origin of improved sensitivity and specificity. J. Mater. Chem. B 2014, 2, 5209–5219.Google Scholar
  70. [70]
    Ng, A. M. H.; Kenry; Teck Lim, C.; Low, H. Y.; Loh, K. P. Highly sensitive reduced graphene oxide microelectrode array sensor. Biosens. Bioelectron. 2015, 65, 265–273.Google Scholar
  71. [71]
    Kook, G.; Lee, S. W.; Lee, H. C.; Cho, I.–J.; Lee, H. J. Neural probes for chronic applications. Micromachines 2016, 7, 179.Google Scholar
  72. [72]
    Jorfi, M.; Skousen, J. L.; Weder, C.; Capadona, J. R. Progress towards biocompatible intracortical microelectrodes for neural interfacing applications. J. Neural Eng. 2014, 12, 011001.Google Scholar
  73. [73]
    Kozai, T. D. Y.; Jaquins–Gerstl, A. S.; Vazquez, A. L.; Michael, A. C.; Cui, X. T. Brain tissue responses to neural implants impact signal sensitivity and intervention strategies. ACS Chem. Neurosci. 2015, 6, 48–67.Google Scholar
  74. [74]
    Takmakov, P.; Ruda, K.; Scott Phillips, K.; Isayeva, I. S.; Krauthamer, V.; Welle, C. G. Rapid evaluation of the durability of cortical neural implants using accelerated aging with reactive oxygen species. J. Neural Eng. 2015, 12, 026003.Google Scholar
  75. [75]
    Seymour, J. P.; Kipke, D. R. Neural probe design for reduced tissue encapsulation in CNS. Biomaterials 2007, 28, 3594–3607.Google Scholar
  76. [76]
    Skousen, J. L.; Merriam, M. E.; Srivannavit, O.; Perlin, G.; Wise, K. D.; Tresco, P. A. Reducing surface area while maintaining implant penetrating profile lowers the brain foreign body response to chronically implanted planar silicon microelectrode arrays. Prog. Brain Res. 2011, 194, 167–180.Google Scholar
  77. [77]
    Karumbaiah, L.; Saxena, T.; Carlson, D.; Patil, K.; Patkar, R.; Gaupp, E. A.; Betancur, M.; Stanley, G. B.; Carin, L.; Bellamkonda, R. V. Relationship between intracortical electrode design and chronic recording function. Biomaterials 2013, 34, 8061–8074.Google Scholar
  78. [78]
    Guitchounts, G.; Markowitz, J. E.; Liberti, W. A.; Gardner, T. J. A carbon–fiber electrode array for long–term neural recording. J. Neural Eng. 2013, 10, 046016.Google Scholar
  79. [79]
    Vitale, F.; Summerson, S. R.; Aazhang, B.; Kemere, C.; Pasquali, M. Neural stimulation and recording with bidirectional, soft carbon nanotube fiber microelectrodes. ACS Nano 2015, 9, 4465–4474.Google Scholar
  80. [80]
    Mercanzini, A.; Cheung, K.; Buhl, D. L.; Boers, M.; Maillard, A.; Colin, P.; Bensadoun, J.–C.; Bertsch, A.; Renaud, P. Demonstration of cortical recording using novel flexible polymer neural probes. Sensor. Actuat. A: Phys. 2008, 143, 90–96.Google Scholar
  81. [81]
    Wu, F.; Tien, L. W.; Chen, F.; Berke, J. D.; Kaplan, D. L.; Yoon, E. Silk–backed structural optimization of high–density flexible intracortical neural probes. J. Microelectromech. Syst. 2015, 24, 62–69.Google Scholar
  82. [82]
    Du, Z. J.; Kolarcik, C. L.; Kozai, T. D. Y.; Luebben, S. D.; Sapp, S. A.; Zheng, X. S.; Nabity, J. A.; Cui, X. T. Ultrasoft microwire neural electrodes improve chronic tissue integration. Acta Biomater. 2017, 53, 46–58.Google Scholar
  83. [83]
    Sohal, H. S.; Clowry, G. J.; Jackson, A.; O’Neill, A.; Baker, S. N. Mechanical flexibility reduces the foreign body response to long–term implanted microelectrodes in rabbit cortex. PLoS One 2016, 11, e0165606.Google Scholar
  84. [84]
    Guo, L.; Guvanasen, G. S.; Liu, X.; Tuthill, C.; Nichols, T. R.; DeWeerth, S. P. A PDMS–based integrated stretchable microelectrode array (isMEA) for neural and muscular surface interfacing. IEEE Trans. Biomed. Circuits Syst. 2013, 7, 1–10.Google Scholar
  85. [85]
    Liu, J.; Xie, C.; Dai, X. H.; Jin, L. H.; Zhou, W.; Lieber, C. M. Multifunctional three–dimensional macroporous nanoelectronic networks for smart materials. Proc. Natl. Acad. Sci. USA 2013, 110, 6694–6699.Google Scholar
  86. [86]
    Liu, J.; Fu, T. M.; Cheng, Z. G.; Hong, G. S.; Zhou, T.; Jin, L. H.; Duvvuri, M.; Jiang, Z.; Kruskal, P.; Xie, C. et al. Syringe–injectable electronics. Nat. Nanotechnol. 2015, 10, 629–636.Google Scholar
  87. [87]
    Fu, T.–M.; Hong, G. S.; Zhou, T.; Schuhmann, T. G.; Viveros, R. D.; Lieber, C. M. Stable long–term chronic brain mapping at the single–neuron level. Nat. Methods 2016, 13, 875–882.Google Scholar
  88. [88]
    Luan, L.; Sullender, C. T.; Li, X.; Zhao, Z. T.; Zhu, H. L.; Wei, X. L.; Xie, C.; Dunn, A. K. Nanoelectronics enabled chronic multimodal neural platform in a mouse ischemic model. J. Neurosci. Methods 2018, 295, 68–76.Google Scholar
  89. [89]
    Zhang, H. N.; Patel, P. R.; Xie, Z. X.; Swanson, S. D.; Wang, X. D.; Kotov, N. A. Tissue–compliant neural implants from microfabricated carbon nanotube multilayer composite. ACS Nano 2013, 7, 7619–7629.Google Scholar
  90. [90]
    Henze, D. A.; Borhegyi, Z.; Csicsvari, J.; Mamiya, A.; Harris, K. D.; Buzsáki, G. Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J. Neurophysiol. 2000, 84, 390–400.Google Scholar
  91. [91]
    Du, J. G.; Blanche, T. J.; Harrison, R. R.; Lester, H. A.; Masmanidis, S. C. Multiplexed, high density electrophysiology with nanofabricated neural probes. PLoS One 2011, 6, e26204.Google Scholar
  92. [92]
    Marblestone, A. H.; Zamft, B. M.; Maguire, Y. G.; Shapiro, M. G.; Cybulski, T. R.; Glaser, J. I.; Amodei, D.; Stranges, P. B.; Kalhor, R.; Dalrymple, D. A. et al. Physical principles for scalable neural recording. Front. Comput. Neurosci. 2013, 7, 137.Google Scholar
  93. [93]
    Camuñas–Mesa, L. A.; Quiroga, R. Q. A detailed and fast model of extracellular recordings. Neural Comput. 2013, 25, 1191–1212.Google Scholar
  94. [94]
    Pedreira, C.; Martinez, J.; Ison, M. J.; Quiroga, R. Q. How many neurons can we see with current spike sorting algorithms? J. Neurosci. Methods 2012, 211, 58–65.Google Scholar
  95. [95]
    Guo, L.; DeWeerth, S. P. An effective lift–off method for patterning high–density gold interconnects on an elastomeric substrate. Small 2010, 6, 2847–2852.Google Scholar
  96. [96]
    Khodagholy, D.; Doublet, T.; Quilichini, P.; Gurfinkel, M.; Leleux, P.; Ghestem, A.; Ismailova, E.; Hervé, T.; Sanaur, S.; Bernard, C. et al. In vivo recordings of brain activity using organic transistors. Nat. Commun. 2013, 4, 1575.Google Scholar
  97. [97]
    Viventi, J.; Kim, D.–H.; Vigeland, L.; Frechette, E. S.; Blanco, J. A.; Kim, Y.–S.; Avrin, A. E.; Tiruvadi, V. R.; Hwang, S.–W.; Vanleer, A. C. et al. Flexible, foldable, actively multiplexed, high–density electrode array for mapping brain activity in vivo. Nat. Neurosci. 2011, 14, 1599–1605.Google Scholar
  98. [98]
    Rios, G.; Lubenov, E. V.; Chi, D.; Roukes, M. L.; Siapas, A. G. Nanofabricated neural probes for dense 3–D recordings of brain activity. Nano Lett. 2016, 16, 6857–6862.Google Scholar
  99. [99]
    Scholvin, J.; Kinney, J. P.; Bernstein, J. G.; Moore–Kochlacs, C.; Kopell, N.; Fonstad, C. G.; Boyden, E. S. Close–packed silicon microelectrodes for scalable spatially oversampled neural recording. IEEE Trans. Biomed. Eng. 2016, 63, 120–130.Google Scholar
  100. [100]
    Wu, F.; Stark, E.; Ku, P.–C.; Wise, K. D.; Buzsáki, G.; Yoon, E. Monolithically integrated μLEDs on silicon neural probes for high–resolution optogenetic studies in behaving animals. Neuron 2015, 88, 1136–1148.Google Scholar
  101. [101]
    Wei, X. L.; Luan, L.; Zhao, Z. T.; Li, X.; Zhu, H. L.; Potnis, O.; Xie, C. Nanofabricated ultraflexible electrode arrays for high–density intracortical recording. Adv. Sci. 2018, 1700625.Google Scholar
  102. [102]
    Lopez, C. M.; Andrei, A.; Mitra, S.; Welkenhuysen, M.; Eberle, W.; Bartic, C.; Puers, R.; Yazicioglu, R. F.; Gielen, G. G. E. An implantable 455–active–electrode 52–channel CMOS neural probe. IEEE J. Solid–St. Circ. 2014, 49, 248–261.Google Scholar
  103. [103]
    Lopez, C. M.; Putzeys, J.; Raducanu, B. C.; Ballini, M.; Wang, S. W.; Andrei, A.; Rochus, V.; Vandebriel, R.; Severi, S.; Hoof, C. V. et al. A neural probe with up to 966 electrodes and up to 384 configurable channels in 0.13 μm SOI CMOS. IEEE Trans. Biomed. Circuits Syst. 2017, 11, 510–522.Google Scholar
  104. [104]
    Jun, J. J.; Steinmetz, N. A.; Siegle, J. H.; Denman, D. J.; Bauza, M.; Barbarits, B.; Lee, A. K.; Anastassiou, C. A.; Andrei, A.; Aydın, Ç. et al. Fully integrated silicon probes for high–density recording of neural activity. Nature 2017, 551, 232–236.Google Scholar
  105. [105]
    Kruss, S.; Salem, D. P.; Vuković, L.; Lima, B.; Vander Ende, E.; Boyden, E. S.; Strano, M. S. High–resolution imaging of cellular dopamine efflux using a fluorescent nanosensor array. Proc. Natl. Acad. Sci. USA 2017, 114, 1789–1794.Google Scholar
  106. [106]
    Beyene, A. G.; McFarlane, I. R.; Pinals, R. L.; Landry, M. P. Stochastic simulation of dopamine neuromodulation for implementation of fluorescent neurochemical probes in the striatal extracellular space. ACS Chem. Neurosci. 2017, 8, 2275–2289.Google Scholar
  107. [107]
    Obien, M. E. J.; Deligkaris, K.; Bullmann, T.; Bakkum, D. J.; Frey, U. Revealing neuronal function through microelectrode array recordings. Front. Neurosci. 2015, 8, 423.Google Scholar
  108. [108]
    Seymour, J. P.; Wu, F.; Wise, K. D.; Yoon, E. State–ofthe–art MEMS and microsystem tools for brain research. Microsyst. Nanoeng. 2017, 3, 16066.Google Scholar
  109. [109]
    Grienberger, C.; Konnerth, A. Imaging calcium in neurons. Neuron 2012, 73, 862–885.Google Scholar
  110. [110]
    Peterka, D. S.; Takahashi, H.; Yuste, R. Imaging voltage in neurons. Neuron 2011, 69, 9–21.Google Scholar
  111. [111]
    Rowland, C. E.; Susumu, K.; Stewart, M. H.; Oh, E.; Mäkinen, A. J.; O’Shaughnessy, T. J.; Kushto, G.; Wolak, M. A.; Erickson, J. S.; Efros, A. L. et al. Electric field modulation of semiconductor quantum dot photoluminescence: Insights into the design of robust voltage–sensitive cellular imaging probes. Nano Lett. 2015, 15, 6848–6854.Google Scholar
  112. [112]
    Alivisatos, A. P. Semiconductor clusters, nanocrystals, and quantum dots. Science 1996, 271, 933–937.Google Scholar
  113. [113]
    Empedocles, S. A.; Bawendi, M. G. Quantum–confined stark effect in single CdSe nanocrystallite quantum dots. Science 1997, 278, 2114–2117.Google Scholar
  114. [114]
    Marshall, J. D.; Schnitzer, M. J. Optical strategies for sensing neuronal voltage using quantum dots and other semiconductor nanocrystals. ACS Nano 2013, 7, 4601–4609.Google Scholar
  115. [115]
    Park, K.; Weiss, S. Design rules for membrane–embedded voltage–sensing nanoparticles. Biophys. J. 2017, 112, 703–713.Google Scholar
  116. [116]
    Knöpfel, T.; Díez–García, J.; Akemann, W. Optical probing of neuronal circuit dynamics: Genetically encoded versus classical fluorescent sensors. Trends Neurosci. 2006, 29, 160–166.Google Scholar
  117. [117]
    Tsytsarev, V.; Liao, L. D.; Kong, K. V.; Liu, Y. H.; Erzurumlu, R. S.; Olivo, M.; Thakor, N. V. Recent progress in voltage–sensitive dye imaging for neuroscience. J. Nanosci. Nanotechnol. 2014, 14, 4733–4744.Google Scholar
  118. [118]
    Tsytsarev, V.; Pope, D.; Pumbo, E.; Yablonskii, A.; Hofmann, M. Study of the cortical representation of whisker directional deflection using voltage–sensitive dye optical imaging. NeuroImage 2010, 53, 233–238.Google Scholar
  119. [119]
    Eriksson, D.; Wunderle, T.; Schmidt, K. Visual cortex combines a stimulus and an error–like signal with a proportion that is dependent on time, space, and stimulus contrast. Front. Syst. Neurosci. 2012, 6, 26.Google Scholar
  120. [120]
    Grinvald, A.; Salzberg, B. M.; Cohen, L. B. Simultaneous recording from several neurones in an invertebrate central nervous system. Nature 1977, 268, 140–142.Google Scholar
  121. [121]
    Cohen, L. B.; Salzberg, B. M.; Grinvald, A. Optical methods for monitoring neuron activity. Annu. Rev. Neurosci. 1978, 1, 171–182.Google Scholar
  122. [122]
    Grandy, T. H.; Greenfield, S. A.; Devonshire, I. M. An evaluation of in vivo voltage–sensitive dyes: Pharmacological side effects and signal–to–noise ratios after effective removal of brain–pulsation artifacts. J. Neurophysiol. 2012, 108, 2931–2945.Google Scholar
  123. [123]
    Nag, O. K.; Stewart, M. H.; Deschamps, J. R.; Susumu, K.; Oh, E.; Tsytsarev, V.; Tang, Q. G.; Efros, A. L.; Vaxenburg, R.; Black, B. J. et al. Quantum dot–peptide–fullerene bioconjugates for visualization of in vitro and in vivo cellular membrane potential. ACS Nano 2017, 11, 5598–5613.Google Scholar
  124. [124]
    Nakai, J.; Ohkura, M.; Imoto, K. A high signal–to–noise Ca2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 2001, 19, 137–141.Google Scholar
  125. [125]
    Nagai, T.; Yamada, S.; Tominaga, T.; Ichikawa, M.; Miyawaki, A. Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc. Natl. Acad. Sci. USA 2004, 101, 10554–10559.Google Scholar
  126. [126]
    Inoue, M.; Takeuchi, A.; Horigane, S.; Ohkura, M.; Gengyo–Ando, K.; Fujii, H.; Kamijo, S.; Takemoto–Kimura, S.; Kano, M.; Nakai, J. et al. Rational design of a high–affinity, fast, red calcium indicator R–CaMP2. Nat. Methods 2015, 12, 64–70.Google Scholar
  127. [127]
    Akemann, W.; Mutoh, H.; Perron, A.; Rossier, J.; Knöpfel, T. Imaging brain electric signals with genetically targeted voltage–sensitive fluorescent proteins. Nat. Methods 2010, 7, 643–649.Google Scholar
  128. [128]
    Miyawaki, A.; Llopis, J.; Heim, R.; McCaffery, J. M.; Adams, J. A.; Ikura, M.; Tsien, R. Y. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 1997, 388, 882–887.Google Scholar
  129. [129]
    Burgoyne, R. D. Neuronal calcium sensor proteins: Generating diversity in neuronal Ca2+ signalling. Nat. Rev. Neurosci. 2007, 8, 182–193.Google Scholar
  130. [130]
    Heim, N.; Griesbeck, O. Genetically encoded indicators of cellular calcium dynamics based on troponin C and green fluorescent protein. J. Biol. Chem. 2004, 279, 14280–14286.Google Scholar
  131. [131]
    Tian, L.; Hires, S. A.; Mao, T. Y.; Huber, D.; Chiappe, M. E.; Chalasani, S. H.; Petreanu, L.; Akerboom, J.; McKinney, S. A.; Schreiter, E. R. et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 2009, 6, 875–881.Google Scholar
  132. [132]
    Ahrens, M. B.; Orger, M. B.; Robson, D. N.; Li, J. M.; Keller, P. J. Whole–brain functional imaging at cellular resolution using light–sheet microscopy. Nat. Methods 2013, 10, 413–420.Google Scholar
  133. [133]
    Chen, T. W.; Wardill, T. J.; Sun, Y.; Pulver, S. R.; Renninger, S. L.; Baohan, A.; Schreiter, E. R.; Kerr, R. A.; Orger, M. B.; Jayaraman, V. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499, 295–300.Google Scholar
  134. [134]
    Barretto, R. P. J.; Gillis–Smith, S.; Chandrashekar, J.; Yarmolinsky, D. A.; Schnitzer, M. J.; Ryba, N. J. P.; Zuker, C. S. The neural representation of taste quality at the periphery. Nature 2015, 517, 373–376.Google Scholar
  135. [135]
    Heim, N.; Garaschuk, O.; Friedrich, M. W.; Mank, M.; Milos, R. I.; Kovalchuk, Y.; Konnerth, A.; Griesbeck, O. Improved calcium imaging in transgenic mice expressing a troponin C–based biosensor. Nat. Methods 2007, 4, 127–129.Google Scholar
  136. [136]
    Palmer, A. E.; Giacomello, M.; Kortemme, T.; Hires, S. A.; Lev–Ram, V.; Baker, D.; Tsien, R. Y. Ca2+ indicators based on computationally redesigned calmodulin–peptide pairs. Chem. Biol. 2006, 13, 521–530.Google Scholar
  137. [137]
    Horikawa, K.; Yamada, Y.; Matsuda, T.; Kobayashi, K.; Hashimoto, M.; Matsu–ura, T.; Miyawaki, A.; Michikawa, T.; Mikoshiba, K.; Nagai, T. Spontaneous network activity visualized by ultrasensitive Ca2+ indicators, yellow Cameleon–Nano. Nat. Methods 2010, 7, 729–732.Google Scholar
  138. [138]
    Dreosti, E.; Odermatt, B.; Dorostkar, M. M.; Lagnado, L. A genetically encoded reporter of synaptic activity in vivo. Nat. Methods 2009, 6, 883–889.Google Scholar
  139. [139]
    Zhao, Y. X.; Araki, S.; Wu, J. H.; Teramoto, T.; Chang, Y. F.; Nakano, M.; Abdelfattah, A. S.; Fujiwara, M.; Ishihara, T.; Nagai, T. et al. An expanded palette of genetically encoded Ca2+ indicators. Science 2011, 333, 1888–1891.Google Scholar
  140. [140]
    Mank, M.; Santos, A. F.; Direnberger, S.; Mrsic–Flogel, T. D.; Hofer, S. B.; Stein, V.; Hendel, T.; Reiff, D. F.; Levelt, C.; Borst, A. et al. A genetically encoded calcium indicator for chronic in vivo two–photon imaging. Nat. Methods 2008, 5, 805–811.Google Scholar
  141. [141]
    Xu, Y. X.; Zou, P.; Cohen, A. E. Voltage imaging with genetically encoded indicators. Curr. Opin. Chem. Biol. 2017, 39, 1–10.Google Scholar
  142. [142]
    Jin, L.; Han, Z.; Platisa, J.; Wooltorton, J. R.; Cohen, L. B.; Pieribone, V. A. Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 2012, 75, 779–785.Google Scholar
  143. [143]
    Cao, G.; Platisa, J.; Pieribone, V. A.; Raccuglia, D.; Kunst, M.; Nitabach, M. N. Genetically targeted optical electrophysiology in intact neural circuits. Cell 2013, 154, 904–913.Google Scholar
  144. [144]
    St–Pierre, F.; Marshall, J. D.; Yang, Y.; Gong, Y. Y.; Schnitzer, M. J.; Lin, M. Z. High–fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat. Neurosci. 2014, 17, 884–889.Google Scholar
  145. [145]
    Lam, A. J.; St–Pierre, F.; Gong, Y. Y.; Marshall, J. D.; Cranfill, P. J.; Baird, M. A.; McKeown, M. R.; Wiedenmann, J.; Davidson, M. W.; Schnitzer, M. J. et al. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 2012, 9, 1005–1012.Google Scholar
  146. [146]
    Siegel, M. S.; Isacoff, E. Y. A genetically encoded optical probe of membrane voltage. Neuron 1997, 19, 735–741.Google Scholar
  147. [147]
    Ataka, K.; Pieribone, V. A. A genetically targetable fluorescent probe of channel gating with rapid kinetics. Biophys. J. 2002, 82, 509–516.Google Scholar
  148. [148]
    Sakai, R.; Repunte–Canonigo, V.; Raj, C. D.; Knöpfel, T. Design and characterization of a DNA–encoded, voltagesensitive fluorescent protein. Eur. J. Neurosci. 2001, 13, 2314–2318.Google Scholar
  149. [149]
    Guerrero, G.; Siegel, M. S.; Roska, B.; Loots, E.; Isacoff, E. Y. Tuning FlaSh: Redesign of the dynamics, voltage range, and color of the genetically encoded optical sensor of membrane potential. Biophys. J. 2002, 83, 3607–3618.Google Scholar
  150. [150]
    Baker, B. J.; Jin, L.; Han, Z.; Cohen, L. B.; Popovic, M.; Platisa, J.; Pieribone, V. Genetically encoded fluorescent voltage sensors using the voltage–sensing domain of Nematostella and Danio phosphatases exhibit fast kinetics. J. Neurosci. Methods 2012, 208, 190–196.Google Scholar
  151. [151]
    Lundby, A.; Mutoh, H.; Dimitrov, D.; Akemann, W.; Knöpfel, T. Engineering of a genetically encodable fluorescent voltage sensor exploiting fast Ci–VSP voltagesensing movements. PLoS One 2008, 3, e2514.Google Scholar
  152. [152]
    Perron, A.; Mutoh, H.; Launey, T.; Knöpfel, T. Red–shifted voltage–sensitive fluorescent proteins. Chem. Biol. 2009, 16, 1268–1277.Google Scholar
  153. [153]
    Akemann, W.; Mutoh, H.; Perron, A.; Park, Y. K.; Iwamoto, Y.; Knöpfel, T. Imaging neural circuit dynamics with a voltage–sensitive fluorescent protein. J. Neurophysiol. 2012, 108, 2323–2337.Google Scholar
  154. [154]
    Kralj, J. M.; Hochbaum, D. R.; Douglass, A. D.; Cohen, A. E. Electrical spiking in Escherichia coli probed with a fluorescent voltage–indicating protein. Science 2011, 333, 345–348.Google Scholar
  155. [155]
    Kralj, J. M.; Douglass, A. D.; Hochbaum, D. R.; Maclaurin, D.; Cohen, A. E. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 2011, 9, 90–95.Google Scholar
  156. [156]
    Hochbaum, D. R.; Zhao, Y. X.; Farhi, S. L.; Klapoetke, N.; Werley, C. A.; Kapoor, V.; Zou, P.; Kralj, J. M.; Maclaurin, D.; Smedemark–Margulies, N. et al. All–optical electrophysiology in mammalian neurons using engineered microbial rhodopsins. Nat. Methods 2014, 11, 825–833.Google Scholar
  157. [157]
    Wang, K.; Fishman, H. A.; Dai, H. J.; Harris, J. S. Neural stimulation with a carbon nanotube microelectrode array. Nano Lett. 2006, 6, 2043–2048.Google Scholar
  158. [158]
    Tsang, W. M.; Stone, A. L.; Otten, D.; Aldworth, Z. N.; Daniel, T. L.; Hildebrand, J. G.; Levine, R. B.; Voldman, J. Insect–machine interface: A carbon nanotube–enhanced flexible neural probe. J. Neurosci. Methods 2012, 204, 355–365.Google Scholar
  159. [159]
    Yi, W. W.; Chen, C. Y.; Feng, Z. Y.; Xu, Y.; Zhou, C. P.; Masurkar, N.; Cavanaugh, J.; Ming–Cheng Cheng, M. A flexible and implantable microelectrode arrays using hightemperature grown vertical carbon nanotubes and a biocompatible polymer substrate. Nanotechnology 2015, 26, 125301.Google Scholar
  160. [160]
    Panescu, D. Emerging technologies wireless communication systems for implantable medical devices]. IEEE Eng. Med. Biol. Mag. 2008, 27, 96–101.Google Scholar
  161. [161]
    Beric, A.; Kelly, P. J.; Rezai, A.; Sterio, D.; Mogilner, A.; Zonenshayn, M.; Kopell, B. Complications of deep brain stimulation surgery. Stereotact. Funct. Neurosurg. 2001, 77, 73–78.Google Scholar
  162. [162]
    Eom, K.; Hwang, S.; Yun, S.; Byun, K. M.; Jun, S. B.; Kim, S. J. Photothermal activation of astrocyte cells using localized surface plasmon resonance of gold nanorods. J. Biophotonics 2017, 10, 486–493.Google Scholar
  163. [163]
    Chen, R.; Romero, G.; Christiansen, M. G.; Mohr, A.; Anikeeva, P. Wireless magnetothermal deep brain stimulation. Science 2015, 347, 1477–1480.Google Scholar
  164. [164]
    Barolet, D. Light–emitting diodes (LEDs) in dermatology. Semin. Cutan. Med. Surg. 2008, 27, 227–238.Google Scholar
  165. [165]
    Legon, W.; Sato, T. F.; Opitz, A.; Mueller, J.; Barbour, A.; Williams, A.; Tyler, W. J. Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans. Nat. Neurosci. 2014, 17, 322–329.Google Scholar
  166. [166]
    Deng, Z.–D.; Lisanby, S. H.; Peterchev, A. V. Electric field depth–focality tradeoff in transcranial magnetic stimulation: Simulation comparison of 50 coil designs. Brain Stimul. 2013, 6, 1–13.Google Scholar
  167. [167]
    Paviolo, C.; Haycock, J. W.; Cadusch, P. J.; McArthur, S. L.; Stoddart, P. R. Laser exposure of gold nanorods can induce intracellular calcium transients. J. Biophotonics 2014, 7, 761–765.Google Scholar
  168. [168]
    Choi, Y. K.; Lee, D. H.; Seo, Y. K.; Jung, H.; Park, J. K.; Cho, H. Stimulation of neural differentiation in human bone marrow mesenchymal stem cells by extremely low–frequency electromagnetic fields incorporated with MNPs. Appl. Biochem. Biotechnol. 2014, 174, 1233–1245.Google Scholar
  169. [169]
    Nakatsuji, H.; Numata, T.; Morone, N.; Kaneko, S.; Mori, Y.; Imahori, H.; Murakami, T. Thermosensitive ion channel activation in single neuronal cells by using surfaceengineered plasmonic nanoparticles. Angew. Chem., Int. Ed. 2015, 54, 11725–11729.Google Scholar
  170. [170]
    Bareket, L.; Waiskopf, N.; Rand, D.; Lubin, G.; David–Pur, M.; Ben–Dov, J.; Roy, S.; Eleftheriou, C.; Sernagor, E.; Cheshnovsky, O. et al. Semiconductor nanorod–carbon nanotube biomimetic films for wire–free photostimulation of blind retinas. Nano Lett. 2014, 14, 6685–6692.Google Scholar
  171. [171]
    Guduru, R.; Liang, P.; Hong, J.; Rodzinski, A.; Hadjikhani, A.; Horstmyer, J.; Levister, E.; Khizroev, S. Magnetoelectric “spin” on stimulating the brain. Nanomedicine 2015, 10, 2051–2061.Google Scholar
  172. [172]
    Marino, A.; Arai, S.; Hou, Y. Y.; Sinibaldi, E.; Pellegrino, M.; Chang, Y. T.; Mazzolai, B.; Mattoli, V.; Suzuki, M.; Ciofani, G. Piezoelectric nanoparticle–assisted wireless neuronal stimulation. ACS Nano 2015, 9, 7678–7689.Google Scholar
  173. [173]
    Carvalho–de–Souza, J. L.; Treger, J. S.; Dang, B. B.; Kent, S. B. H.; Pepperberg, D. R.; Bezanilla, F. Photosensitivity of neurons enabled by cell–targeted gold nanoparticles. Neuron 2015, 86, 207–217.Google Scholar
  174. [174]
    Shah, S.; Liu, J. J.; Pasquale, N.; Lai, J. P.; McGowan, H.; Pang, Z. P.; Lee, K. B. Hybrid upconversion nanomaterials for optogenetic neuronal control. Nanoscale 2015, 7, 16571–16577.Google Scholar
  175. [175]
    Tay, A.; Kunze, A.; Murray, C.; Di Carlo, D. Induction of calcium influx in cortical neural networks by nanomagnetic forces. ACS Nano 2016, 10, 2331–2341.Google Scholar
  176. [176]
    Catterall, W. A. Structure and function of voltage–gated ion channels. Annu. Rev. Biochem. 1995, 64, 493–531.Google Scholar
  177. [177]
    Bean, B. P. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 2007, 8, 451–465.Google Scholar
  178. [178]
    Bareket–Keren, L.; Hanein, Y. Novel interfaces for light directed neuronal stimulation: Advances and challenges. Int. J. Nanomedicine 2014, 9, 65–83.Google Scholar
  179. [179]
    Smith, A. M.; Mancini, M. C.; Nie, S. M. Second window for in vivo imaging. Nat. Nanotechnol. 2009, 4, 710–711.Google Scholar
  180. [180]
    Del Bonis–O’Donnell, J. T.; Page, R. H.; Beyene, A. G.; Tindall, E. G.; McFarlane, I. R.; Landry, M. P. Dual near–infrared two–photon microscopy for deep–tissue dopamine nanosensor imaging. Adv. Funct. Mater. 2017, 27, 1702112.Google Scholar
  181. [181]
    Lugo, K.; Miao, X. Y.; Rieke, F.; Lin, L. Y. Remote switching of cellular activity and cell signaling using light in conjunction with quantum dots. Biomed. Opt. Express 2012, 3, 447–454.Google Scholar
  182. [182]
    Gomez, N.; Winter, J. O.; Shieh, F.; Saunders, A. E.; Korgel, B. A.; Schmidt, C. E. Challenges in quantum dot–neuron active interfacing. Talanta 2005, 67, 462–471.Google Scholar
  183. [183]
    Winter, J. O.; Liu, T. Y.; Korgel, B. A.; Schmidt, C. E. Recognition molecule directed interfacing between semiconductor quantum dots and nerve cells. Adv. Mater. 2001, 13, 1673–1677.Google Scholar
  184. [184]
    Winter, J. O.; Gomez, N.; Korgel, B. A.; Schmidt, C. E. Quantum dots for electrical stimulation of neural cells. Proceedings of SPIE 2005, 5705, 235–246.Google Scholar
  185. [185]
    Pappas, T. C.; Wickramanyake, W. M. S.; Jan, E.; Motamedi, M.; Brodwick, M.; Kotov, N. A. Nanoscale engineering of a cellular interface with semiconductor nanoparticle films for photoelectric stimulation of neurons. Nano Lett. 2007, 7, 513–519.Google Scholar
  186. [186]
    Molokanova, E.; Bartel, J. A.; Zhao, W. W.; Naasani, I.; Ignatius, M. J.; Treadway, J. A.; Savtchenko, A. Quantum dots move beyond fluorescence imaging. Biophot. Int. 2008, 15, 26–31.Google Scholar
  187. [187]
    Yue, K.; Guduru, R.; Hong, J.; Liang, P.; Nair, M.; Khizroev, S. Magneto–electric nano–particles for non–invasive brain stimulation. PLoS One 2012, 7, e44040.Google Scholar
  188. [188]
    Tyler, W. J.; Tufail, Y.; Finsterwald, M.; Tauchmann, M. L.; Olson, E. J.; Majestic, C. Remote excitation of neuronal circuits using low–intensity, low–frequency ultrasound. PLoS One 2008, 3, e3511.Google Scholar
  189. [189]
    Wang, Y. C.; Wu, Y.; Quadri, F.; Prox, J. D.; Guo, L. Cytotoxicity of ZnO nanowire arrays on excitable cells. Nanomaterial 2017, 7, 80.Google Scholar
  190. [190]
    Ciofani, G.; Danti, S.; D’Alessandro, D.; Ricotti, L.; Moscato, S.; Bertoni, G.; Falqui, A.; Berrettini, S.; Petrini, M.; Mattoli, V. et al. Enhancement of neurite outgrowth in neuronal–like cells following boron nitride nanotubemediated stimulation. ACS Nano 2010, 4, 6267–6277.Google Scholar
  191. [191]
    Ricotti, L.; Fujie, T.; Vazão, H.; Ciofani, G.; Marotta, R.; Brescia, R.; Filippeschi, C.; Corradini, I.; Matteoli, M.; Mattoli, V. et al. Boron nitride nanotube–mediated stimulation of cell co–culture on micro–engineered hydrogels. PLoS One 2013, 8, e71707.Google Scholar
  192. [192]
    Genchi, G. G.; Ceseracciu, L.; Marino, A.; Labardi, M.; Marras, S.; Pignatelli, F.; Bruschini, L.; Mattoli, V.; Ciofani, G. P(VDF–TrFE)/BaTiO3 nanoparticle composite films mediate piezoelectric stimulation and promote differentiation of SH–SY5Y neuroblastoma cells. Adv. Healthc. Mater. 2016, 5, 1808–1820.Google Scholar
  193. [193]
    Rojas, C.; Tedesco, M.; Massobrio, P.; Marino, A.; Ciofani, G.; Martinoia, S.; Raiteri, R. Acoustic stimulation can induce a selective neural network response mediated by piezoelectric nanoparticles. J. Neural Eng. 2018, 15, 036016.Google Scholar
  194. [194]
    Marino, A.; Barsotti, J.; de Vito, G.; Filippeschi, C.; Mazzolai, B.; Piazza, V.; Labardi, M.; Mattoli, V.; Ciofani, G. Twophoton lithography of 3D nanocomposite piezoelectric scaffolds for cell stimulation. ACS Appl. Mater. Interfaces 2015, 7, 25574–25579.Google Scholar
  195. [195]
    Hoop, M.; Chen, X. Z.; Ferrari, A.; Mushtaq, F.; Ghazaryan, G.; Tervoort, T.; Poulikakos, D.; Nelson, B.; Pané, S. Ultrasound–mediated piezoelectric differentiation of neuron–like PC12 cells on PVDF membranes. Sci. Rep. 2017, 7, 4028.Google Scholar
  196. [196]
    Lee, Y.–S.; Collins, G.; Arinzeh, T. L. Neurite extension of primary neurons on electrospun piezoelectric scaffolds. Acta Biomater. 2011, 7, 3877–3886.Google Scholar
  197. [197]
    Eustis, S.; El–Sayed, M. A. Why gold nanoparticles are more precious than pretty gold: Noble metal surface plasmon resonance and its enhancement of the radiative and nonradiative properties of nanocrystals of different shapes. Chem. Soc. Rev. 2006, 35, 209–217.Google Scholar
  198. [198]
    Shapiro, M. G.; Homma, K.; Villarreal, S.; Richter, C. P.; Bezanilla, F. Infrared light excites cells by changing their electrical capacitance. Nat. Commun. 2012, 3, 736.Google Scholar
  199. [199]
    Benham, C. D.; Gunthorpe, M. J.; Davis, J. B. TRPV channels as temperature sensors. Cell Calcium 2003, 33, 479–487.Google Scholar
  200. [200]
    Paviolo, C.; Haycock, J. W.; Yong, J.; Yu, A.; Stoddart, P. R.; McArthur, S. L. Laser exposure of gold nanorods can increase neuronal cell outgrowth. Biotechnol. Bioeng. 2013, 110, 2277–2291.Google Scholar
  201. [201]
    Yong, J.; Needham, K.; Brown, W. G. A.; Nayagam, B. A.; McArthur, S. L.; Yu, A. M.; Stoddart, P. R. Gold–nanorod–assisted near–infrared stimulation of primary auditory neurons. Adv. Healthc. Mater. 2014, 3, 1862–1868.Google Scholar
  202. [202]
    Eom, K.; Kim, J.; Choi, J. M.; Kang, T.; Chang, J. W.; Byun, K. M.; Jun, S. B.; Kim, S. J. Enhanced infrared neural stimulation using localized surface plasmon resonance of gold nanorods. Small 2014, 10, 3853–3857.Google Scholar
  203. [203]
    Yoo, S.; Hong, S.; Choi, Y.; Park, J. H.; Nam, Y. Photothermal inhibition of neural activity with nearinfrared–sensitive nanotransducers. ACS Nano 2014, 8, 8040–8049.Google Scholar
  204. [204]
    Lavoie–Cardinal, F.; Salesse, C.; Bergeron, É.; Meunier, M.; De Koninck, P. Gold nanoparticle–assisted all optical localized stimulation and monitoring of Ca2+ signaling in neurons. Sci. Rep. 2016, 6, 20619.Google Scholar
  205. [205]
    Eom, K.; Im, C.; Hwang, S.; Eom, S.; Kim, T. S.; Jeong, H. S.; Kim, K. H.; Byun, K. M.; Jun, S. B.; Kim, S. J. Synergistic combination of near–infrared irradiation and targeted gold nanoheaters for enhanced photothermal neural stimulation. Biomed. Opt. Express 2016, 7, 1614–1625.Google Scholar
  206. [206]
    Yoo, S.; Kim, R.; Park, J. H.; Nam, Y. Electro–optical neural platform integrated with nanoplasmonic inhibition interface. ACS Nano 2016, 10, 4274–4281.Google Scholar
  207. [207]
    Bazard, P.; Frisina, R. D.; Walton, J. P.; Bhethanabotla, V. R. Nanoparticle–based plasmonic transduction for modulation of electrically excitable cells. Sci. Rep. 2017, 7, 7803.Google Scholar
  208. [208]
    Tay, A.; Di Carlo, D. Magnetic nanoparticle–based mechanical stimulation for restoration of mechano–sensitive ion channel equilibrium in neural networks. Nano Lett. 2017, 17, 886–892.Google Scholar
  209. [209]
    Stanley, S. A.; Gagner, J. E.; Damanpour, S.; Yoshida, M.; Dordick, J. S.; Friedman, J. M. Radio–wave heating of iron oxide nanoparticles can regulate plasma glucose in mice. Science 2012, 336, 604–608.Google Scholar
  210. [210]
    Stanley, S. A.; Sauer, J.; Kane, R. S.; Dordick, J. S.; Friedman, J. M. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat. Med. 2015, 21, 92–98.Google Scholar
  211. [211]
    Boyden, E. S.; Zhang, F.; Bamberg, E.; Nagel, G.; Deisseroth, K. Millisecond–timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8, 1263–1268.Google Scholar
  212. [212]
    Lin, J. Y.; Knutsen, P. M.; Muller, A.; Kleinfeld, D.; Tsien, R. Y. ReaChR: A red–shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat. Neurosci. 2013, 16, 1499–1508.Google Scholar
  213. [213]
    Klapoetke, N. C.; Murata, Y.; Kim, S. S.; Pulver, S. R.; Birdsey–Benson, A.; Cho, Y. K.; Morimoto, T. K.; Chuong, A. S.; Carpenter, E. J.; Tian, Z. J. et al. Independent optical excitation of distinct neural populations. Nat. Methods 2014, 11, 338–346.Google Scholar
  214. [214]
    Chuong, A. S.; Miri, M. L.; Busskamp, V.; Matthews, G. A.; Acker, L. C.; Sørensen, A. T.; Young, A.; Klapoetke, N. C.; Henninger, M. A.; Kodandaramaiah, S. B. et al. Noninvasive optical inhibition with a red–shifted microbial rhodopsin. Nat. Neurosci. 2014, 17, 1123–1129.Google Scholar
  215. [215]
    Pansare, V. J.; Hejazi, S.; Faenza, W. J.; Prud’homme, R. K. Review of long–wavelength optical and NIR imaging materials: Contrast agents, fluorophores, and multifunctional nano carriers. Chem. Mater. 2012, 24, 812–827.Google Scholar
  216. [216]
    Hososhima, S.; Yuasa, H.; Ishizuka, T.; Hoque, M. R.; Yamashita, T.; Yamanaka, A.; Sugano, E.; Tomita, H.; Yawo, H. Near–infrared (NIR) up–conversion optogenetics. Sci. Rep. 2015, 5, 16533.Google Scholar
  217. [217]
    Bansal, A.; Liu, H. C.; Jayakumar, M. K. G.; Andersson–Engels, S.; Zhang, Y. Quasi–continuous wave near–infrared excitation of upconversion nanoparticles for optogenetic manipulation of C. elegans. Small 2016, 12, 1732–1743.Google Scholar
  218. [218]
    He, L.; Zhang, Y. W; Ma, G. L.; Tan, P.; Li, Z. J.; Zang, S. B.; Wu, X.; Jing, J.; Fang, S. H.; Zhou, L. J. et al. Near–infrared photoactivatable control of Ca2+ signaling and optogenetic immunomodulation. eLife 2015, 4, e10024.Google Scholar
  219. [219]
    Wu, X.; Zhang, Y. W.; Takle, K.; Bilsel, O.; Li, Z. J.; Lee, H.; Zhang, Z. J.; Li, D. S.; Fan, W.; Duan, C. Y. et al. Dye–sensitized core/active shell upconversion nanoparticles for optogenetics and bioimaging applications. ACS Nano 2016, 10, 1060–1066.Google Scholar
  220. [220]
    Huang, K.; Dou, Q. Q.; Loh, X. J. Nanomaterial mediated optogenetics: Opportunities and challenges. RSC Adv. 2016, 6, 60896–60906.Google Scholar
  221. [221]
    El Haj, A. J.; Hughes, S.; Dobson, J. Manipulation of ion channels using magnetic micro–and nanoparticle cytometry. Comp. Biochem. Phys. A 2003, 134, S110.Google Scholar
  222. [222]
    Hughes, S.; El Haj, A. J.; Dobson, J. Magnetic micro–and nanoparticle mediated activation of mechanosensitive ion channels. Med. Eng. Phys. 2005, 27, 754–762.Google Scholar
  223. [223]
    Kunze, A.; Tseng, P.; Godzich, C.; Murray, C.; Caputo, A.; Schweizer, F. E.; Di Carlo, D. Engineering cortical neuron polarity with nanomagnets on a chip. ACS Nano 2015, 9, 3664–3676.Google Scholar
  224. [224]
    Etoc, F.; Vicario, C.; Lisse, D.; Siaugue, J. M.; Piehler, J.; Coppey, M.; Dahan, M. Magnetogenetic control of protein gradients inside living cells with high spatial and temporal resolution. Nano Lett. 2015, 15, 3487–3494.Google Scholar
  225. [225]
    Wang, N.; Butler, J. P.; Ingber, D. E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 1993, 260, 1124–1127.Google Scholar
  226. [226]
    Wang, N.; Ingber, D. E. Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 1994, 66, 1281–1289.Google Scholar
  227. [227]
    Wang, N.; Ingber, D. E. Probing transmembrane mechanical coupling and cytomechanics using magnetic twisting cytometry. Biochem. Cell Biol. 1995, 73, 327–335.Google Scholar
  228. [228]
    Glogauer, M.; Ferrier, J.; McCulloch, C. A. Magnetic fields applied to collagen–coated ferric oxide beads induce stretch–activated Ca2+ flux in fibroblasts. Am. J. Physiol. 1995, 269, C1093–1104.Google Scholar
  229. [229]
    Hughes, S.; McBain, S.; Dobson, J.; El Haj, A. J. Selective activation of mechanosensitive ion channels using magnetic particles. J. R. Soc. Interface 2008, 5, 855–863.Google Scholar
  230. [230]
    Matthews, B. D.; Thodeti, C. K.; Tytell, J. D.; Mammoto, A.; Overby, D. R.; Ingber, D. E. Ultra–rapid activation of TRPV4 ion channels by mechanical forces applied to cell surface β1 integrins. Integr. Biol. 2010, 2, 435–442.Google Scholar
  231. [231]
    Mannix, R. J.; Kumar, S.; Cassiola, F.; Montoya–Zavala, M.; Feinstein, E.; Prentiss, M.; Ingber, D. E. Nanomagnetic actuation of receptor–mediated signal transduction. Nat. Nanotechnol. 2008, 3, 36–40.Google Scholar
  232. [232]
    Cho, M. H.; Lee, E. J.; Son, M.; Lee, J. H.; Yoo, D.; Kim, J.; Park, S. W.; Shin, J. S.; Cheon, J. A magnetic switch for the control of cell death signalling in in vitro and in vivo systems. Nat. Mater. 2012, 11, 1038–1043.Google Scholar
  233. [233]
    Bharde, A. A.; Palankar, R.; Fritsch, C.; Klaver, A.; Kanger, J. S.; Jovin, T. M.; Arndt–Jovin, D. J. Magnetic nanoparticles as mediators of ligand–free activation of EGFR signaling. PLoS One 2013, 8, e68879.Google Scholar
  234. [234]
    Steketee, M. B.; Moysidis, S. N.; Jin, X. L.; Weinstein, J. E.; Pita–Thomas, W.; Raju, H. B.; Iqbal, S.; Goldberg, J. L. Nanoparticle–mediated signaling endosome localization regulates growth cone motility and neurite growth. Proc. Natl. Acad. Sci. USA 2011, 108, 19042–19047.Google Scholar
  235. [235]
    Tay, A. K.; Dhar, M.; Pushkarsky, I.; Di Carlo, D. Research highlights: Manipulating cells inside and out. Lab Chip 2015, 15, 2533–2537.Google Scholar
  236. [236]
    Miesenböck, G. Optogenetic control of cells and circuits. Annu. Rev. Cell. Dev. Biol. 2011, 27, 731–758.Google Scholar
  237. [237]
    Deisseroth, K. Optogenetics: 10 years of microbial opsins in neuroscience. Nat. Neurosci. 2015, 18, 1213–1225.Google Scholar
  238. [238]
    Boyden, E. S. Optogenetics and the future of neuroscience. Nat. Neurosci. 2015, 18, 1200–1201.Google Scholar
  239. [239]
    Boyden, E. S. A history of optogenetics: The development of tools for controlling brain circuits with light. F1000 Biol. Rep. 2011, 3, 11.Google Scholar
  240. [240]
    Knöpfel, T.; Boyden, E. S. Optogenetics: Tools for controlling and monitoring neuronal activity preface. Prog. Brain Res. 2012, 196, VII–VIII.Google Scholar
  241. [241]
    Deisseroth, K. Optogenetics. Nat. Methods 2011, 8, 26–29.Google Scholar
  242. [242]
    Gerits, A.; Vanduffel, W. Optogenetics in primates: A shining future? Trends Genet. 2013, 29, 403–411.Google Scholar
  243. [243]
    Madisen, L.; Mao, T. Y.; Koch, H.; Zhuo, J. M.; Berenyi, A.; Fujisawa, S.; Hsu, Y. W. A.; Garcia, A. J., 3rd; Gu, X.; Zanella, S. et al. A toolbox of Cre–dependent optogenetic transgenic mice for light–induced activation and silencing. Nat. Neurosci. 2012, 15, 793–802.Google Scholar
  244. [244]
    Zhang, F.; Vierock, J.; Yizhar, O.; Fenno, L. E.; Tsunoda, S.; Kianianmomeni, A.; Prigge, M.; Berndt, A.; Cushman, J.; Polle, J. et al. The microbial opsin family of optogenetic tools. Cell 2011, 147, 1446–1457.Google Scholar
  245. [245]
    Gautier, A.; Gauron, C.; Volovitch, M.; Bensimon, D.; Jullien, L.; Vriz, S. How to control proteins with light in living systems. Nat. Chem. Biol. 2014, 10, 533–541.Google Scholar
  246. [246]
    Land, B. B.; Brayton, C. E.; Furman, K. E.; Lapalombara, Z.; DiLeone, R. J. Optogenetic inhibition of neurons by internal light production. Front. Behav. Neurosci. 2014, 8, 108.Google Scholar
  247. [247]
    Nihongaki, Y.; Kawano, F.; Nakajima, T.; Sato, M. Photoactivatable CRISPR–Cas9 for optogenetic genome editing. Nat. Biotechnol. 2015, 33, 755–760.Google Scholar
  248. [248]
    Nihongaki, Y.; Yamamoto, S.; Kawano, F.; Suzuki, H.; Sato, M. CRISPR–Cas9–based photoactivatable transcription system. Chem. Biol. 2015, 22, 169–174.Google Scholar
  249. [249]
    Gradinaru, V.; Zhang, F.; Ramakrishnan, C.; Mattis, J.; Prakash, R.; Diester, I.; Goshen, I.; Thompson, K. R.; Deisseroth, K. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141, 154–165.Google Scholar
  250. [250]
    Zhang, F.; Wang, L. P.; Brauner, M.; Liewald, J. F.; Kay, K.; Watzke, N.; Wood, P. G.; Bamberg, E.; Nagel, G.; Gottschalk, A. et al. Multimodal fast optical interrogation of neural circuitry. Nature 2007, 446, 633–639.Google Scholar
  251. [251]
    Gradinaru, V.; Thompson, K. R.; Deisseroth, K. eNpHR: A natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol. 2008, 36, 129–139.Google Scholar
  252. [252]
    Zhao, S. L.; Cunha, C.; Zhang, F.; Liu, Q.; Gloss, B.; Deisseroth, K.; Augustine, G. J.; Feng, G. P. Improved expression of halorhodopsin for light–induced silencing of neuronal activity. Brain Cell Biol. 2008, 36, 141–154.Google Scholar
  253. [253]
    Zhang, F.; Prigge, M.; Beyrière, F.; Tsunoda, S. P.; Mattis, J.; Yizhar, O.; Hegemann, P.; Deisseroth, K. Red–shifted optogenetic excitation: A tool for fast neural control derived from Volvox carteri. Nat. Neurosci. 2008, 11, 631–633.Google Scholar
  254. [254]
    Yizhar, O.; Fenno, L. E.; Prigge, M.; Schneider, F.; Davidson, T. J.; O’Shea, D. J.; Sohal, V. S.; Goshen, I.; Finkelstein, J.; Paz, J. T. et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011, 477, 171–178.Google Scholar
  255. [255]
    Chow, B. Y.; Han, X.; Dobry, A. S.; Qian, X. F.; Chuong, A. S.; Li, M. J.; Henninger, M. A.; Belfort, G. M.; Lin, Y. X.; Monahan, P. E. et al. High–performance genetically targetable optical neural silencing by light–driven proton pumps. Nature 2010, 463, 98–102.Google Scholar
  256. [256]
    Mattis, J.; Tye, K. M.; Ferenczi, E. A.; Ramakrishnan, C.; O'Shea, D. J.; Prakash, R.; Gunaydin, L. A.; Hyun, M.; Fenno, L. E.; Gradinaru, V. et al. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat. Methods 2011, 9, 159–172.Google Scholar
  257. [257]
    Wietek, J.; Wiegert, J. S.; Adeishvili, N.; Schneider, F.; Watanabe, H.; Tsunoda, S. P.; Vogt, A.; Elstner, M.; Oertner, T. G.; Hegemann, P. Conversion of channelrhodopsin into a light–gated chloride channel. Science 2014, 344, 409–412.Google Scholar
  258. [258]
    Govorunova, E. G.; Sineshchekov, O. A.; Janz, R.; Liu, X. Q.; Spudich, J. L. Natural light–gated anion channels: A family of microbial rhodopsins for advanced optogenetics. Science 2015, 349, 647–650.Google Scholar
  259. [250]
    Lin, J. Y.; Lin, M. Z.; Steinbach, P.; Tsien, R. Y. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 2009, 96, 1803–1814.Google Scholar
  260. [260]
    Berndt, A.; Schoenenberger, P.; Mattis, J.; Tye, K. M.; Deisseroth, K.; Hegemann, P.; Oertner, T. G. Highefficiency channelrhodopsins for fast neuronal stimulation at low light levels. Proc. Natl. Acad. Sci. USA 2011, 108, 7595–7600.Google Scholar
  261. [261]
    Matsuzaki, M.; Ellis–Davies, G. C.; Nemoto, T.; Miyashita, Y.; Iino, M.; Kasai, H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001, 4, 1086–1092.Google Scholar
  262. [262]
    Gorostiza, P.; Isacoff, E. Y. Optical switches for remote and noninvasive control of cell signaling. Science 2008, 322, 395–399.Google Scholar
  263. [263]
    Dobson, J. Remote control of cellular behaviour with magnetic nanoparticles. Nat. Nanotechnol. 2008, 3, 139–143.Google Scholar
  264. [264]
    Monzel, C.; Vicario, C.; Piehler, J.; Coppey, M.; Dahan, M. Magnetic control of cellular processes using biofunctional nanoparticles. Chem. Sci. 2017, 8, 7330–7338.Google Scholar
  265. [265]
    Patel, A. J.; Honoré, E. Properties and modulation of mammalian 2P domain K+ channels. Trends Neurosci. 2001, 24, 339–346.Google Scholar
  266. [266]
    Wheeler, M. A.; Smith, C. J.; Ottolini, M.; Barker, B. S.; Purohit, A. M.; Grippo, R. M.; Gaykema, R. P.; Spano, A. J.; Beenhakker, M. P.; Kucenas, S. et al. Genetically targeted magnetic control of the nervous system. Nat. Neurosci. 2016, 19, 756–761.Google Scholar
  267. [267]
    McKemy, D. D.; Neuhausser, W. M.; Julius, D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 2002, 416, 52–58.Google Scholar
  268. [268]
    Stanley, S. A.; Kelly, L.; Latcha, K. N.; Schmidt, S. F.; Yu, X. F.; Nectow, A. R.; Sauer, J.; Dyke, J. P.; Dordick, J. S.; Friedman, J. M. Bidirectional electromagnetic control of the hypothalamus regulates feeding and metabolism. Nature 2016, 531, 647–650.Google Scholar
  269. [269]
    Qin, S. Y.; Yin, H.; Yang, C. L.; Dou, Y. F.; Liu, Z. M.; Zhang, P.; Yu, H.; Huang, Y. L.; Feng, J.; Hao, J. F. et al. A magnetic protein biocompass. Nat. Mater. 2016, 15, 217–226.Google Scholar
  270. [270]
    Long, X. Y.; Ye, J.; Zhao, D.; Zhang, S. J. Magnetogenetics: Remote non–invasive magnetic activation of neuronal activity with a magnetoreceptor. Sci. Bull. 2015, 60, 2107–2119.Google Scholar
  271. [271]
    Ibsen, S.; Tong, A.; Schutt, C.; Esener, S.; Chalasani, S. H. Sonogenetics is a non–invasive approach to activating neurons in Caenorhabditis elegans. Nat. Commun. 2015, 6, 8264.Google Scholar
  272. [272]
    Kubanek, J.; Shi, J. Y.; Marsh, J.; Chen, D.; Deng, C. R.; Cui, J. M. Ultrasound modulates ion channel currents. Sci. Rep. 2016, 6, 24170.Google Scholar
  273. [273]
    Spira, M. E.; Hai, A. Multi–electrode array technologies for neuroscience and cardiology. Nat. Nanotechnol. 2013, 8, 83–94.Google Scholar
  274. [274]
    Berger, T. W.; Baudry, M.; Brinton, R. D.; Liaw, J.–S.; Marmarelis, V. Z.; Park, A. Y.; Sheu, B. J.; Tanguay, A. R. Brain–implantable biomimetic electronics as the next era in neural prosthetics. Proc. IEEE 2001, 89, 993–1012.Google Scholar
  275. [275]
    Berger, T. W.; Hampson, R. E.; Song, D.; Goonawardena, A.; Marmarelis, V. Z.; Deadwyler, S. A. A cortical neural prosthesis for restoring and enhancing memory. J. Neural Eng. 2011, 8, 046017.Google Scholar
  276. [276]
    Ezzyat, Y.; Wanda, P. A.; Levy, D. F.; Kadel, A.; Aka, A.; Pedisich, I.; Sperling, M. R.; Sharan, A. D.; Lega, B. C.; Burks, A. et al. Closed–loop stimulation of temporal cortex rescues functional networks and improves memory. Nat. Commun. 2018, 9, 365.Google Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringThe Ohio State UniversityColumbusUSA
  2. 2.Department of Biomedical EngineeringThe University of Texas at AustinAustinUSA
  3. 3.Department of Electrical and Computer EngineeringThe Ohio State UniversityColumbusUSA
  4. 4.Key Laboratory of Flexible Electronics and Institute of Advanced Materials, Jiangsu National Synergetic Innovation Center for Advanced MaterialsNanjing Tech UniversityNanjingChina
  5. 5.Biomedical Sciences Graduate ProgramThe Ohio State UniversityColumbusUSA
  6. 6.Department of NeuroscienceThe Ohio State UniversityColumbusUSA

Personalised recommendations