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Biomimetic approaches toward smart bio-hybrid systems

Abstract

Bio-integrated materials and devices can blur the interfaces between living and artificial systems. Microfluidics, bioelectronics, and engineered nanostructures, with close interactions with biology at the cellular or tissue levels, have already yielded a spectrum of new applications. Many new designs emerge, including of organ-on-a-chip systems, biodegradable implants, electroceutical devices, minimally invasive neuro-prosthetic tools, and soft robotics. In this review, we highlight a few recent advances of the fabrication and application of smart bio-hybrid systems, with a particular emphasis on the three-dimensional (3D) bio-integrated devices that mimic the 3D feature of tissue scaffolds. Moreover,neurons integrated with engineered nanostructures for wireless neuromodulation and dynamic neural output are briefly discussed. We also discuss the progress in the construction of cell-enabled soft robotics, where a tight coupling of the synthetic and biological parts is crucial for efficient function. Finally, we summarize the approaches for enhancing bio-integration with biomimetic micro- and nanostructures.

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References

  1. Hyam, J. A.; Kringelbach, M. L.; Silburn, P. A.; Aziz, T. Z.; Green, A. L. The autonomic effects of deep brain stimulation—a therapeutic opportunity. Nat. Rev. Neurol. 2012, 8, 391–400.

    Article  Google Scholar 

  2. Jackson, A.; Zimmermann, J. B. Neural interfaces for the brain and spinal cord—restoring motor function. Nat. Rev. Neurol. 2012, 8, 690–699.

    Article  Google Scholar 

  3. Birmingham, K.; Gradinaru, V.; Anikeeva, P.; Grill, W. M.; Pikov, V.; McLaughlin, B.; Pasricha, P.; Weber, D.; Ludwig, K.; Famm, K. Bioelectronic medicines: A research roadmap. Nat. Rev. Drug Discov. 2014, 13, 399–400.

    Article  Google Scholar 

  4. Fox, D. The shock tactics set to shake up immunology. Nature 2017, 545, 20–22.

    Article  Google Scholar 

  5. 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.

    Article  Google Scholar 

  6. Gunasekera, B.; Saxena, T.; Bellamkonda, R.; Karumbaiah, L. Intracortical recording interfaces: Current challenges to chronic recording function. ACS Chem. Neurosci. 2015, 6, 68–83.

    Article  Google Scholar 

  7. Lacour, S. P.; Courtine, G.; Guck, J. Materials and technologies for soft implantable neuroprostheses. Nat. Rev. Mater. 2016, 1, 16063.

    Article  Google Scholar 

  8. Jeong, J. W.; Shin, G.; Park, S. I.; Yu, K. J.; Xu, L. Z.; Rogers, J. A. Soft materials in neuroengineering for hard problems in neuroscience. Neuron 2015, 86, 175–186.

    Article  Google Scholar 

  9. Choi, S.; Lee, H.; Ghaffari, R.; Hyeon, T.; Kim, D. H. Recent advances in flexible and stretchable bio-electronic devices integrated with nanomaterials. Adv. Mater. 2016, 28, 4203–4218.

    Article  Google Scholar 

  10. Green, R.; Abidian, M. R. Conducting polymers for neural prosthetic and neural interface applications. Adv. Mater. 2015, 27, 7620–7637.

    Article  Google Scholar 

  11. Tian, B. Z.; Lieber, C. M. Synthetic nanoelectronic probes for biological cells and tissues. Annu. Rev. Anal. Chem. 2013, 6, 31–51.

    Article  Google Scholar 

  12. Duan, X. J.; Fu, T. M.; Liu, J.; Lieber, C. M. Nanoelectronics-biology frontier: From nanoscopic probes for action potential recording in live cells to three-dimensional cyborg tissues. Nano Today 2013, 8, 351–373.

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. Cohen-Karni, T.; Langer, R.; Kohane, D. S. The smartest materials: The future of nanoelectronics in medicine. ACS Nano 2012, 6, 6541–6545.

    Article  Google Scholar 

  15. Esch, E. W.; Bahinski, A.; Huh, D. Organs-on-chips at the frontiers of drug discovery. Nat. Rev. Drug Discov. 2015, 14, 248–260.

    Article  Google Scholar 

  16. Guan, A.; Hamilton, P.; Wang, Y.; Gorbet, M.; Li, Z. Y.; Phillips, K. S. Medical devices on chips. Nat. Biomed. Eng. 2017, 1, 0045.

    Article  Google Scholar 

  17. Feinberg, A. W. Biological soft robotics. Annu. Rev. Biomed. Eng. 2015, 17, 243–265.

    Article  Google Scholar 

  18. Patino, T.; Mestre, R.; Sánchez, S. Miniaturized soft bio-hybrid robotics: A step forward into healthcare applications. Lab Chip 2016, 16, 3626–3630.

    Article  Google Scholar 

  19. Dvir, T.; Timko, B. P.; Kohane, D. S.; Langer, R. Nanotechnological strategies for engineering complex tissues. Nat. Nanotechnol. 2011, 6, 13–22.

    Article  Google Scholar 

  20. Bajaj, P.; Schweller, R. M.; Khademhosseini, A.; West, J. L.; Bashir, R. 3D biofabrication strategies for tissue engineering and regenerative medicine. Annu. Rev. Biomed. Eng. 2014, 16, 247–276.

    Article  Google Scholar 

  21. Tian, B. Z.; Liu, J.; Dvir, T.; Jin, L. H.; Tsui, J. H.; Qing, Q.; Suo, Z. G.; Langer, R.; Kohane, D. S.; Lieber, C. M. Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. Nat. Mater. 2012, 11, 986–994.

    Article  Google Scholar 

  22. Dai, X. C.; Zhou, W.; Gao, T.; Liu, J.; Lieber, C. M. Three-dimensional mapping and regulation of action potential propagation in nanoelectronics-innervated tissues. Nat. Nanotechnol. 2016, 11, 776–782.

    Article  Google Scholar 

  23. Liu, J.; Xie, C.; Dai, X.; Jin, L.; Zhou, W.; Lieber, C. M. Multifunctional three-dimensional macroporous nanoelectronic networks for smart materials. Proc. Natl. Acad. Sci. USA 2013, 110, 6694–6699.

    Article  Google Scholar 

  24. Feiner, R.; Engel, L.; Fleischer, S.; Malki, M.; Gal, I.; Shapira, A.; Shacham-Diamand, Y.; Dvir, T. Engineered hybrid cardiac patches with multifunctional electronics for online monitoring and regulation of tissue function. Nat. Mater. 2016, 15, 679–685.

    Article  Google Scholar 

  25. Zhang, Y. H.; Zhang, F.; Yan, Z.; Ma, Q.; Li, X. L.; Huang, Y. G.; Rogers, J. A. Printing, folding and assembly methods for forming 3D mesostructures in advanced materials. Nat. Rev. Mater. 2017, 2, 17019.

    Article  Google Scholar 

  26. Murphy, S. V.; Atala, A. 3D bioprinting of tissues and organs. Nat. Biotechnol. 2014, 32, 773–785.

    Article  Google Scholar 

  27. Do, A. V.; Khorsand, B.; Geary, S. M.; Salem, A. K. 3D printing of scaffolds for tissue regeneration applications. Adv. Healthc. Mater. 2015, 4, 1742–1762.

    Article  Google Scholar 

  28. Kong, Y. L.; Gupta, M. K.; Johnson, B. N.; McAlpine, M. C. 3D printed bionic nanodevices. Nano Today 2016, 11, 330–350.

    Article  Google Scholar 

  29. Shin, S. R.; Farzad, R.; Tamayol, A.; Manoharan, V.; Mostafalu, P.; Zhang, Y. S.; Akbari, M.; Jung, S. M.; Kim, D.; Comotto, M. et al. A bioactive carbon nanotube-based ink for printing 2D and 3D flexible electronics. Adv. Mater. 2016, 28, 3280–3289.

    Article  Google Scholar 

  30. Lind, J. U.; Busbee, T. A.; Valentine, A. D.; Pasqualini, F. S.; Yuan, H. Y.; Yadid, M.; Park, S. J.; Kotikian, A.; Nesmith, A. P.; Campbell, P. H. et al. Instrumented cardiac microphysiological devices via multimaterial three-dimensional printing. Nat. Mater. 2017, 16, 303–308.

    Article  Google Scholar 

  31. Hwang, S. W.; Tao, H.; Kim, D. H.; Cheng, H. Y.; Song, J. K.; Rill, E.; Brenckle, M. A.; Panilaitis, B.; Won, S. M.; Kim, Y. S. et al. A physically transient form of silicon electronics. Science 2012, 337, 1640–1644.

    Article  Google Scholar 

  32. Kang, S. K.; Murphy, R. K. J.; Hwang, S. W.; Lee, S. M.; Harburg, D. V.; Krueger, N. A.; Shin, J.; Gamble, P.; Cheng, H. Y.; Yu, S. et al. Bioresorbable silicon electronic sensors for the brain. Nature 2016, 530, 71–76.

    Article  Google Scholar 

  33. Yu, K. J.; Kuzum, D.; Hwang, S. W.; Kim, B. H.; Juul, H.; Kim, N. H.; Won, S. M.; Chiang, K.; Trumpis, M.; Richardson, A. G. et al. Bioresorbable silicon electronics for transient spatiotemporal mapping of electrical activity from the cerebral cortex. Nat. Mater. 2016, 15, 782–791.

    Article  Google Scholar 

  34. Zhang, B. Y.; Montgomery, M.; Chamberlain, M. D.; Ogawa, S.; Korolj, A.; Pahnke, A.; Wells, L. A.; Massé, S.; Kim, J.; Reis, L. et al. Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat. Mater. 2016, 15, 669–678.

    Article  Google Scholar 

  35. Fleischer, S.; Shapira, A.; Feiner, R.; Dvir, T. Modular assembly of thick multifunctional cardiac patches. Proc. Natl. Acad. Sci. USA 2017, 114, 1898–1903.

    Article  Google Scholar 

  36. Cogan, S. F. Neural stimulation and recording electrodes. Annu. Rev. Biomed. Eng. 2008, 10, 275–309.

    Article  Google Scholar 

  37. 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.

    Article  Google Scholar 

  38. 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.

    Article  Google Scholar 

  39. 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.

    Article  Google Scholar 

  40. Chen, R.; Canales, A.; Anikeeva, P. Neural recording and modulation technologies. Nat. Rev. Mater. 2017, 2, 16093.

    Article  Google Scholar 

  41. Tee, B. C. K.; Chortos, A.; Berndt, A.; Nguyen, A. K.; Tom, A.; McGuire, A.; Lin, Z. C.; Tien, K.; Bae, W. G.; Wang, H. L. et al. A skin-inspired organic digital mechanoreceptor. Science 2015, 350, 313–316.

    Article  Google Scholar 

  42. Kim, C. K.; Adhikari, A.; Deisseroth, K. Integration of optogenetics with complementary methodologies in systems neuroscience. Nat. Rev. Neurosci. 2017, 18, 222–235.

    Article  Google Scholar 

  43. Rivnay, J.; Wang, H. L.; Fenno, L.; Deisseroth, K.; Malliaras, G. G. Next-generation probes, particles, and proteins for neural interfacing. Sci. Adv. 2017, 3, e1601649.

    Article  Google Scholar 

  44. Carvalho-de-Souza, J. L.; Treger, J. S.; Dang, B.; Kent, S. B. H.; Pepperberg, D. R.; Bezanilla, F. Photosensitivity of neurons enabled by cell-targeted gold nanoparticles. Neuron 2015, 86, 207–217.

    Article  Google Scholar 

  45. 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.

    Article  Google Scholar 

  46. Yoo, S.; Hong, S.; Choi, Y.; Park, J. H.; Nam, Y. Photothermal inhibition of neural activity with near-infrared-sensitive nanotransducers. ACS Nano 2014, 8, 8040–8049.

    Article  Google Scholar 

  47. Lyu, Y.; Xie, C.; Chechetka, S. A.; Miyako, E.; Pu, K. Semiconducting polymer nanobioconjugates for targeted photothermal activation of neurons. J. Am. Chem. Soc. 2016, 138, 9049–9052.

    Article  Google Scholar 

  48. Jiang, Y. W.; Carvalho-de-Souza, J. L.; Wong, R. C. S.; Luo, Z. Q.; Isheim, D.; Zuo, X. B.; Nicholls, A. W.; Jung, I. W.; Yue, J. P.; Liu, D. J. et al. Heterogeneous silicon mesostructures for lipid-supported bioelectric interfaces. Nat. Mater. 2016, 15, 1023–1030.

    Article  Google Scholar 

  49. 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.

    Article  Google Scholar 

  50. 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.

    Article  Google Scholar 

  51. Chen, R.; Romero, G.; Christiansen, M. G.; Mohr, A.; Anikeeva, P. Wireless magnetothermal deep brain stimulation. Science 2015, 347, 1477–1480.

    Article  Google Scholar 

  52. Munshi, R.; Qadri, S. M.; Zhang, Q.; Castellanos Rubio, I.; Del Pino, P.; Pralle, A. Magnetothermal genetic deep brain stimulation of motor behaviors in awake, freely moving mice. eLife 2017, 6, e27069.

    Article  Google Scholar 

  53. Rus, D.; Tolley, M. T. Design, fabrication and control of soft robots. Nature 2015, 521, 467–475.

    Article  Google Scholar 

  54. Feinberg, A. W.; Feigel, A.; Shevkoplyas, S. S.; Sheehy, S.; Whitesides, G. M.; Parker, K. K. Muscular thin films for building actuators and powering devices. Science 2007, 317, 1366–1370.

    Article  Google Scholar 

  55. Nawroth, J. C.; Lee, H.; Feinberg, A. W.; Ripplinger, C. M.; McCain, M. L.; Grosberg, A.; Dabiri, J. O.; Parker, K. K. A tissue-engineered jellyfish with biomimetic propulsion. Nat. Biotechnol. 2012, 30, 792–797.

    Article  Google Scholar 

  56. Cvetkovic, C.; Raman, R.; Chan, V.; Williams, B. J.; Tolish, M.; Bajaj, P.; Sakar, M. S.; Asada, H. H.; Saif, M. T. A.; Bashir, R. Three-dimensionally printed biological machines powered by skeletal muscle. Proc. Natl. Acad. Sci. USA 2014, 111, 10125–10130.

    Article  Google Scholar 

  57. Raman, R.; Cvetkovic, C.; Bashir, R. A modular approach to the design, fabrication, and characterization of muscle-powered biological machines. Nat. Protoc. 2017, 12, 519–533.

    Article  Google Scholar 

  58. Cvetkovic, C.; Rich, M. H.; Raman, R.; Kong, H.; Bashir, R. A 3D-printed platform for modular neuromuscular motor units. Microsyst. Nanoeng. 2017, 3, 17015.

    Article  Google Scholar 

  59. Shin, S. R.; Shin, C.; Memic, A.; Shadmehr, S.; Miscuglio, M.; Jung, H. Y.; Jung, S. M.; Bae, H.; Khademhosseini, A.; Tang, X. S. et al. Aligned carbon nanotube-based flexible gel substrates for engineering biohybrid tissue actuators. Adv. Funct. Mater. 2015, 25, 4486–4495.

    Article  Google Scholar 

  60. Raman, R.; Cvetkovic, C.; Uzel, S. G. M.; Platt, R. J.; Sengupta, P.; Kamm, R. D.; Bashir, R. Optogenetic skeletal muscle- powered adaptive biological machines. Proc. Natl. Acad. Sci. USA 2016, 113, 3497–3502.

    Article  Google Scholar 

  61. Park, S. J.; Gazzola, M.; Park, K. S.; Park, S.; Di Santo, V.; Blevins, E. L.; Lind, J. U.; Campbell, P. H.; Dauth, S.; Capulli, A. K. et al. Phototactic guidance of a tissue-engineered soft-robotic ray. Science 2016, 353, 158–162.

    Article  Google Scholar 

  62. Phan, L.; Kautz, R.; Leung, E. M.; Naughton, K. L.; Van Dyke, Y.; Gorodetsky, A. A. Dynamic materials inspired by cephalopods. Chem. Mater. 2016, 28, 6804–6816.

    Article  Google Scholar 

  63. Pikul, J. H.; Li, S.; Bai, H.; Hanlon, R. T.; Cohen, I.; Shepherd, R. F. Stretchable surfaces with programmable 3D texture morphing for synthetic camouflaging skins. Science 2017, 358, 210–214.

    Article  Google Scholar 

  64. Yu, C. J.; Li, Y. H.; Zhang, X.; Huang, X.; Malyarchuk, V.; Wang, S. D.; Shi, Y.; Gao, L.; Su, Y. W.; Zhang, Y. H. et al. Adaptive optoelectronic camouflage systems with designs inspired by cephalopod skins. Proc. Natl. Acad. Sci. USA 2014, 111, 12998–13003.

    Article  Google Scholar 

  65. Li, J.; Celiz, A. D.; Yang, J.; Yang, Q.; Wamala, I.; Whyte, W.; Seo, B. R.; Vasilyev, N. V.; Vlassak, J. J.; Suo, Z. et al. Tough adhesives for diverse wet surfaces. Science 2017, 357, 378–381.

    Article  Google Scholar 

  66. Zhao, Q.; Lee, D. W.; Ahn, B. K.; Seo, S.; Kaufman, Y.; Israelachvili, J. N.; Waite, J. H. Underwater contact adhesion and microarchitecture in polyelectrolyte complexes actuated by solvent exchange. Nat. Mater. 2016, 15, 407–412.

    Article  Google Scholar 

  67. Gebbie, M. A.; Wei, W.; Schrader, A. M.; Cristiani, T. R.; Dobbs, H. A.; Idso, M.; Chmelka, B. F.; Waite, J. H.; Israelachvili, J. N. Tuning underwater adhesion with cation-π interactions. Nat. Chem. 2017, 9, 473–479.

    Article  Google Scholar 

  68. Iturri, J.; Xue, L. J.; Kappl, M.; García-Fernández, L.; Barnes, W. J. P.; Butt, H. J.; del Campo, A. Torrent frog-inspired adhesives: Attachment to flooded surfaces. Adv. Funct. Mater. 2015, 25, 1499–1505.

    Article  Google Scholar 

  69. Drotlef, D. M.; Stepien, L.; Kappl, M.; Barnes, W. J. P.; Butt, H. J.; del Campo, A. Insights into the adhesive mechanisms of tree frogs using artificial mimics. Adv. Funct. Mater. 2013, 23, 1137–1146.

    Article  Google Scholar 

  70. Xue, L. J.; Sanz, B.; Luo, A. Y.; Turner, K. T.; Wang, X.; Tan, D.; Zhang, R.; Du, H.; Steinhart, M.; Mijangos, C. et al. Hybrid surface patterns mimicking the design of the adhesive toe pad of tree frog. ACS Nano 2017, 11, 9711–9719.

    Article  Google Scholar 

  71. Lee, H.; Lee, B. P.; Messersmith, P. B. A reversible wet/dry adhesive inspired by mussels and geckos. Nature 2007, 448, 338–341.

    Article  Google Scholar 

  72. Mahdavi, A.; Ferreira, L.; Sundback, C.; Nichol, J. W.; Chan, E. P.; Carter, D. J. D.; Bettinger, C. J.; Patanavanich, S.; Chignozha, L.; Ben-Joseph, E. et al. A biodegradable and biocompatible gecko-inspired tissue adhesive. Proc. Natl. Acad. Sci. USA 2008, 105, 2307–2312.

    Article  Google Scholar 

  73. Frost, S. J.; Mawad, D.; Higgins, M. J.; Ruprai, H.; Kuchel, R.; Tilley, R. D.; Myers, S.; Hook, J. M.; Lauto, A. Gecko-inspired chitosan adhesive for tissue repair. NPG Asia Mater. 2016, 8, e280.

    Article  Google Scholar 

  74. Luo, Z. Q.; Jiang, Y. W.; Myers, B. D.; Isheim, D.; Wu, J. S.; Zimmerman, J. F.; Wang, Z. G.; Li, Q. Q.; Wang, Y. C.; Chen, X. Q. et al. Atomic gold-enabled three-dimensional lithography for silicon mesostructures. Science 2015, 348, 1451–1455.

    Article  Google Scholar 

  75. Cho, W. K.; Ankrum, J. A.; Guo, D. G.; Chester, S. A.; Yang, S. Y.; Kashyap, A.; Campbell, G. A.; Wood, R. J.; Rijal, R. K.; Karnik, R. et al. Microstructured barbs on the North American porcupine quill enable easy tissue penetration and difficult removal. Proc. Natl. Acad. Sci. USA 2012, 109, 21289–21294.

    Article  Google Scholar 

  76. Yang, S. Y.; O’Cearbhaill, E. D.; Sisk, G. C.; Park, K. M.; Cho, W. K.; Villiger, M.; Bouma, B. E.; Pomahac, B.; Karp, J. M. A bio-inspired swellable microneedle adhesive for mechanical interlocking with tissue. Nat. Commun. 2013, 4, 1702.

    Article  Google Scholar 

  77. Yi, J.; Wang, Y. C.; Jiang, Y. W.; Jung, I. W.; Liu, W. J.; De Andrade, V.; Xu, R. Q.; Parameswaran, R.; Peters, I. R.; Divan, R. et al. 3D calcite heterostructures for dynamic and deformable mineralized matrices. Nat. Commun. 2017, 8, 509.

    Article  Google Scholar 

  78. Chen, Y. C.; Yang, H. T. Octopus-inspired assembly of nanosucker arrays for dry/wet adhesion. ACS Nano 2017, 11, 5332–5338.

    Article  Google Scholar 

  79. Lee, H.; Um, D. S.; Lee, Y.; Lim, S.; Kim, H. J.; Ko, H. Octopus-inspired smart adhesive pads for transfer printing of semiconducting nanomembranes. Adv. Mater. 2016, 28, 7457–7465.

    Article  Google Scholar 

  80. Baik, S.; Kim, D. W.; Park, Y.; Lee, T. J.; Ho Bhang, S.; Pang, C. A wet-tolerant adhesive patch inspired by protuberances in suction cups of octopi. Nature 2017, 546, 396–400.

    Article  Google Scholar 

  81. Pan, F.; Gao, S.; Chen, C.; Song, C.; Zeng, F. Recent progress in resistive random access memories: Materials, switching mechanisms, and performance. Mater. Sci. Eng. R-Rep. 2014, 83, 1–59.

    Article  Google Scholar 

  82. Sheridan, P. M.; Cai, F. X.; Du, C.; Ma, W.; Zhang, Z. Y.; Lu, W. D. Sparse coding with memristor networks. Nat. Nanotechnol. 2017, 12, 784–789.

    Article  Google Scholar 

  83. van de Burgt, Y.; Lubberman, E.; Fuller, E. J.; Keene, S. T.; Faria, G. C.; Agarwal, S.; Marinella, M. J.; Alec Talin, A.; Salleo, A. A non-volatile organic electrochemical device as a low-voltage artificial synapse for neuromorphic computing. Nat. Mater. 2017, 16, 414–418.

    Article  Google Scholar 

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Acknowledgements

Z.Q.L. acknowledges support from the National Natural Science Foundation of China (No. 81771974). B.Z.T. acknowledges a primary support from the University of Chicago Materials Research Science and Engineering Center, which is funded by the National Science Foundation under award number DMR-1420709. B.Z.T. also acknowledges support from the National Institutes of Health (No. NIH 1DP2NS101488).

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Luo, Z., Weiss, D.E., Liu, Q. et al. Biomimetic approaches toward smart bio-hybrid systems. Nano Res. 11, 3009–3030 (2018). https://doi.org/10.1007/s12274-018-2004-1

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  • DOI: https://doi.org/10.1007/s12274-018-2004-1

Keywords

  • bio-integrated device
  • bio-hybrid system
  • biomimetics
  • nano-bio interface