Journal Home > Volume 17 , Issue 2
Nano Research 2024, 17(2): 618-632 https://doi.org/10.1007/s12274-023-6136-6
Review Article | Issue | Published: 03 October 2023

Bioinspired nanotransducers for neuromodulation

Show Author's Information Fan Yang1,2,3,  Xiang Wu1,2,  Sa Cai1,2,  Guosong Hong1,2( )
Department of Materials Science and Engineering, Stanford University, Stanford, CA 94305, USA
Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA 94305, USA
School of Science, Shenzhen Campus of Sun Yat-sen University, Shenzhen 518107, China
Keywords:
neuromodulation, bioinspired synthesis, mechanoluminescence, focused ultrasound, nanotransducers, sono-optogenetics
Topics:
Nano biology
Cite this article:
Yang F, Wu X, Cai S, et al. Bioinspired nanotransducers for neuromodulation. Nano Research, 2024, 17(2): 618-632. https://doi.org/10.1007/s12274-023-6136-6
Download citation
EndNote(RIS)
BibTeX

707

Views

127

Downloads

Citations

3

Crossref

2

WoS

3

Scopus

0

CSCD

Abstract Full text About this article

The field of neuromodulation has experienced significant advancements in the past decade, owing to breakthroughs in disciplines such as materials science, genetics, bioengineering, photonics, and beyond. The convergence of these fields has resulted in the development of nanotransducers, devices that harness the synergies of these diverse disciplines. These nanotransducers, essential for neuromodulation, often draw inspiration from energy conversion processes found in nature for their unique modalities. In this review, we will delve into the latest advancements in wireless neuromodulation facilitated by optical, magnetic, and mechanical nanotransducers. We will examine their working principles, properties, advantages, and limitations in comparison to current methods for deep brain neuromodulation, highlighting the impact of natural systems on their design and functionality. Additionally, we will underscore potential future directions, emphasizing how continued progress in materials science, neuroscience, and bioengineering might expand the horizons of what is achievable with nanotransducer-enabled neuromodulation.


menu
Abstract
Full text
Outline
About this article

Bioinspired nanotransducers for neuromodulation

Show Author's information Fan Yang1,2,3, Xiang Wu1,2, Sa Cai1,2, Guosong Hong1,2( )
Department of Materials Science and Engineering, Stanford University, Stanford, CA 94305, USA
Wu Tsai Neurosciences Institute, Stanford University, Stanford, CA 94305, USA
School of Science, Shenzhen Campus of Sun Yat-sen University, Shenzhen 518107, China

Abstract

The field of neuromodulation has experienced significant advancements in the past decade, owing to breakthroughs in disciplines such as materials science, genetics, bioengineering, photonics, and beyond. The convergence of these fields has resulted in the development of nanotransducers, devices that harness the synergies of these diverse disciplines. These nanotransducers, essential for neuromodulation, often draw inspiration from energy conversion processes found in nature for their unique modalities. In this review, we will delve into the latest advancements in wireless neuromodulation facilitated by optical, magnetic, and mechanical nanotransducers. We will examine their working principles, properties, advantages, and limitations in comparison to current methods for deep brain neuromodulation, highlighting the impact of natural systems on their design and functionality. Additionally, we will underscore potential future directions, emphasizing how continued progress in materials science, neuroscience, and bioengineering might expand the horizons of what is achievable with nanotransducer-enabled neuromodulation.

Keywords: neuromodulation, bioinspired synthesis, mechanoluminescence, focused ultrasound, nanotransducers, sono-optogenetics

References(71)

[1]

Won, S. M.; Song, E. M.; Reeder, J. T.; Rogers, J. A. Emerging modalities and implantable technologies for neuromodulation. Cell 2020, 181, 115–135.
DOI Google Scholar
[2]

Lozano, A. M.; Lipsman, N.; Bergman, H.; Brown, P.; Chabardes, S.; Chang, J. W.; Matthews, K.; McIntyre, C. C.; Schlaepfer, T. E.; Schulder, M. et al. Deep brain stimulation: Current challenges and future directions. Nat. Rev. Neurol. 2019, 15, 148–160.
DOI Google Scholar
[3]

Zhang, F.; Aravanis, A. M.; Adamantidis, A.; De Lecea, L.; Deisseroth, K. Circuit-breakers: Optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 2007, 8, 577–581.
DOI Google Scholar
[4]

Yang, F.; Kim, S. J.; Wu, X.; Cui, H.; Hahn, S. K.; Hong, G. S. Principles and applications of sono-optogenetics. Adv. Drug Delivery Rev. 2023, 194, 114711.
DOI Google Scholar
[5]

Li, X. Y.; Xiong, H. J.; Rommelfanger, N.; Xu, X. Q.; Youn, J.; Slesinger, P. A.; Hong, G. S.; Qin, Z. P. Nanotransducers for wireless neuromodulation. Matter 2021, 4, 1484–1510.
DOI Google Scholar
[6]

Yang, X.; Zhou, T.; Zwang, T. J.; Hong, G. S.; Zhao, Y. L.; Viveros, R. D.; Fu, T. M.; Gao, T.; Lieber, C. M. Bioinspired neuron-like electronics. Nat. Mater. 2019, 18, 510–517.
DOI Google Scholar
[7]

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.
DOI Google Scholar
[8]

Marshel, J. H.; Kim, Y. S.; Machado, T. A.; Quirin, S.; Benson, B.; Kadmon, J.; Raja, C.; Chibukhchyan, A.; Ramakrishnan, C.; Inoue, M. et al. Cortical layer-specific critical dynamics triggering perception. Science 2019, 365, eaaw5202.
DOI Google Scholar
[9]

Hong, G. S.; Antaris, A. L.; Dai, H. J. Near-infrared fluorophores for biomedical imaging. Nat. Biomed. Eng. 2017, 1, 0010.
DOI Google Scholar
[10]

Zhang, F.; Gradinaru, V.; Adamantidis, A. R.; Durand, R.; Airan, R. D.; De Lecea, L.; Deisseroth, K. Optogenetic interrogation of neural circuits: Technology for probing mammalian brain structures. Nat. Protoc. 2010, 5, 439–456.
DOI Google Scholar
[11]

Kim, T. I.; McCall, J. G.; Jung, Y. H.; Huang, X.; Siuda, E. R.; Li, Y. H.; Song, J. Z.; 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.
DOI Google Scholar
[12]

Montgomery, K. L.; Yeh, A. J.; Ho, J. S.; Tsao, V.; Mohan Iyer, S.; Grosenick, L.; Ferenczi, E. A.; Tanabe, Y.; Deisseroth, K.; Delp, S. L. et al. Wirelessly powered, fully internal optogenetics for brain, spinal and peripheral circuits in mice. Nat. Methods 2015, 12, 969–974.
DOI Google Scholar
[13]

Yang, Y. Y.; Wu, M. Z.; Vázquez-Guardado, A.; Wegener, A. J.; Grajales-Reyes, J. G.; Deng, Y. J.; Wang, T. Y.; Avila, R.; Moreno, J. A.; Minkowicz, S. et al. Wireless multilateral devices for optogenetic studies of individual and social behaviors. Nat. Neurosci. 2021, 24, 1035–1045.
DOI Google Scholar
[14]

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.
DOI Google Scholar
[15]

Chen, R.; Gore, F.; Nguyen, Q. A.; Ramakrishnan, C.; Patel, S.; Kim, S. H.; Raffiee, M.; Kim, Y. S.; Hsueh, B.; Krook-Magnusson, E. et al. Deep brain optogenetics without intracranial surgery. Nat. Biotechnol. 2021, 39, 161–164.
DOI Google Scholar
[16]

Bedbrook, C. N.; Yang, K. K.; Robinson, J. E.; Mackey, E. D.; Gradinaru, V.; Arnold, F. H. Machine learning-guided channelrhodopsin engineering enables minimally invasive optogenetics. Nat. Methods 2019, 16, 1176–1184.
DOI Google Scholar
[17]

Gong, X.; Mendoza-Halliday, D.; Ting, J. T.; Kaiser, T.; Sun, X. Y.; Bastos, A. M.; Wimmer, R. D.; Guo, B. L.; Chen, Q.; Zhou, Y. et al. An ultra-sensitive step-function opsin for minimally invasive optogenetic stimulation in mice and macaques. Neuron 2020, 107, 38–51.e8.
DOI Google Scholar
[18]
Deisseroth, K.; Anikeeva, P. Upconversion of light for use in optogenetic methods. U. S. Patent 9, 522, 288, December 20, 2016.
[19]

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.
DOI Google Scholar
[20]

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.
DOI Google Scholar
[21]

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.
DOI Google Scholar
[22]

Pliss, A.; Ohulchanskyy, T. Y.; Chen, G. Y.; Damasco, J.; Bass, C. E.; Prasad, P. N. Subcellular optogenetics enacted by targeted nanotransformers of near-infrared light. ACS Photonics 2017, 4, 806–814.
DOI Google Scholar
[23]

Yadav, K.; Chou, A. C.; Ulaganathan, R. K.; Gao, H. D.; Lee, H. M.; Pan, C. Y.; Chen, Y. T. Targeted and efficient activation of channelrhodopsins expressed in living cells via specifically-bound upconversion nanoparticles. Nanoscale 2017, 9, 9457–9466.
DOI Google Scholar
[24]

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.
DOI Google Scholar
[25]

Ai, X. Z.; Lyu, L.; Zhang, Y.; Tang, Y. X.; Mu, J.; Liu, F.; Zhou, Y. X.; Zuo, Z. H.; Liu, G.; Xing, B. G. Remote regulation of membrane channel activity by site-specific localization of lanthanide-doped upconversion nanocrystals. Angew. Chem., Int. Ed. 2017, 56, 3031–3035.
DOI Google Scholar
[26]

Wang, Y.; Lin, X. D.; Chen, X.; Chen, X.; Xu, Z.; Zhang, W. C.; Liao, Q. H.; Duan, X.; Wang, X.; Liu, M. et al. Tetherless near-infrared control of brain activity in behaving animals using fully implantable upconversion microdevices. Biomaterials 2017, 142, 136–148.
DOI Google Scholar
[27]

Lin, X. D.; Wang, Y.; Chen, X.; Yang, R. H.; Wang, Z. X.; Feng, J. Y.; Wang, H. T.; Lai, K. W. C.; He, J. F.; Wang, F. et al. Multiplexed optogenetic stimulation of neurons with spectrum-selective upconversion nanoparticles. Adv. Healthcare Mater. 2017, 6, 1700446.
DOI Google Scholar
[28]

Lin, X. D.; Chen, X.; Zhang, W. C.; Sun, T. Y.; Fang, P. L.; Liao, Q. H.; Chen, X.; He, J. F.; Liu, M.; Wang, F. et al. Core–shell–shell upconversion nanoparticles with enhanced emission for wireless optogenetic inhibition. Nano Lett. 2018, 18, 948–956.
DOI Google Scholar
[29]

Chen, S.; Weitemier, A. Z.; Zeng, X.; He, L. M.; Wang, X. Y.; Tao, Y. Q.; Huang, A. J. Y.; Hashimotodani, Y.; Kano, M.; Iwasaki, H. et al. Near-infrared deep brain stimulation via upconversion nanoparticle-mediated optogenetics. Science 2018, 359, 679–684.
DOI Google Scholar
[30]

Ma, Y. Q.; Bao, J.; Zhang, Y. W.; Li, Z. J.; Zhou, X. Y.; Wan, C. L.; Huang, L.; Zhao, Y.; Han, G.; Xue, T. Mammalian near-infrared image vision through injectable and self-powered retinal nanoantennae. Cell 2019, 177, 243–255.e15.
DOI Google Scholar
[31]

Ding, H.; Lu, L. H.; Shi, Z.; Wang, D.; Li, L. Z.; Li, X. C.; Ren, Y. Q.; Liu, C. B.; Cheng, D. L.; Kim, H. et al. Microscale optoelectronic infrared-to-visible upconversion devices and their use as injectable light sources. Proc. Natl. Acad. Sci. USA 2018, 115, 6632–6637.
DOI Google Scholar
[32]

Mei, Q. S.; Bansal, A.; Jayakumar, M. K. G.; Zhang, Z. M.; Zhang, J.; Huang, H.; Yu, D. J.; Ramachandra, C. J. A.; Hausenloy, D. J.; Soong, T. W. et al. Manipulating energy migration within single lanthanide activator for switchable upconversion emissions towards bidirectional photoactivation. Nat. Commun. 2019, 10, 4416.
DOI Google Scholar
[33]

Liu, X.; Chen, H. M.; Wang, Y. T.; Si, Y. G.; Zhang, H. X.; Li, X. M.; Zhang, Z. C.; Yan, B.; Jiang, S.; Wang, F. et al. Near-infrared manipulation of multiple neuronal populations via trichromatic upconversion. Nat. Commun. 2021, 12, 5662.
DOI Google Scholar
[34]

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.
DOI Google Scholar
[35]

Lyu, Y.; Xie, C.; Chechetka, S. A.; Miyako, E.; Pu, K. Y. Semiconducting polymer nanobioconjugates for targeted photothermal activation of neurons. J. Am. Chem. Soc. 2016, 138, 9049–9052.
DOI Google Scholar
[36]

Rastogi, S. K.; Garg, R.; Scopelliti, M. G.; Pinto, B. I.; Hartung, J. E.; Kim, S.; Murphey, C. G. E.; Johnson, N.; San Roman, D.; Bezanilla, F. et al. Remote nongenetic optical modulation of neuronal activity using fuzzy graphene. Proc. Natl. Acad. Sci. USA 2020, 117, 13339–13349.
DOI Google Scholar
[37]

Gracheva, E. O.; Ingolia, N. T.; Kelly, Y. M.; Cordero-Morales, J. F.; Hollopeter, G.; Chesler, A. T.; Sánchez, E. E.; Perez, J. C.; Weissman, J. S.; Julius, D. Molecular basis of infrared detection by snakes. Nature 2010, 464, 1006–1011.
DOI Google Scholar
[38]

Li, J. C.; Pu, K. Y. Semiconducting polymer nanomaterials as near-infrared photoactivatable protherapeutics for cancer. Acc. Chem. Res. 2020, 53, 752–762.
DOI Google Scholar
[39]

Wu, X.; Yang, F.; Cai, S.; Pu, K. Y.; Hong, G. S. Nanotransducer-enabled deep-brain neuromodulation with NIR-II light. ACS Nano 2023, 17, 7941–7952.
DOI Google Scholar
[40]

Wu, X.; Jiang, Y. Y.; Rommelfanger, N. J.; Yang, F.; Zhou, Q.; Yin, R. K.; Liu, J. L.; Cai, S.; Ren, W.; Shin, A. et al. Tether-free photothermal deep-brain stimulation in freely behaving mice via wide-field illumination in the near-infrared-II window. Nat. Biomed. Eng. 2022, 6, 754–770.
DOI Google Scholar
[41]

Nakatsuji, H.; Numata, T.; Morone, N.; Kaneko, S.; Mori, Y.; Imahori, H.; Murakami, T. Thermosensitive ion channel activation in single neuronal cells by using surface-engineered plasmonic nanoparticles. Angew. Chem., Int. Ed. 2015, 54, 11725–11729.
DOI Google Scholar
[42]

Nelidova, D.; Morikawa, R. K.; Cowan, C. S.; Raics, Z.; Goldblum, D.; Scholl, H. P. N.; Szikra, T.; Szabo, A.; Hillier, D.; Roska, B. Restoring light sensitivity using tunable near-infrared sensors. Science 2020, 368, 1108–1113.
DOI Google Scholar
[43]

Efros, A. L.; Delehanty, J. B.; Huston, A. L.; Medintz, I. L.; Barbic, M.; Harris, T. D. Evaluating the potential of using quantum dots for monitoring electrical signals in neurons. Nat. Nanotechnol. 2018, 13, 278–288.
DOI Google Scholar
[44]

Yang, F.; Zhang, Q. Z.; Huang, S. Y.; Ma, D. L. Recent advances of near infrared inorganic fluorescent probes for biomedical applications. J. Mater. Chem. B 2020, 8, 7856–7879.
DOI Google Scholar
[45]

Bahmani Jalali, H.; Mohammadi Aria, M.; Dikbas, U. M.; Sadeghi, S.; Ganesh Kumar, B.; Sahin, M.; Kavakli, I. H.; Ow-Yang, C. W.; Nizamoglu, S. Effective neural photostimulation using indium-based type-II quantum dots. ACS Nano 2018, 12, 8104–8114.
DOI Google Scholar
[46]

Karatum, O.; Kaleli, H. N.; Eren, G. O.; Sahin, A.; Nizamoglu, S. Electrical stimulation of neurons with quantum dots via near-infrared light. ACS Nano 2022, 16, 8233–8243.
DOI Google Scholar
[47]

Yang, F.; Skripka, A.; Tabatabaei, M. S.; Hong, S. H.; Ren, F. Q.; Huang, Y.; Oh, J. K.; Martel, S.; Liu, X. Y.; Vetrone, F. et al. Magnetic photoluminescent nanoplatform built from large-pore mesoporous silica. Chem. Mater. 2019, 31, 3201–3210.
DOI Google Scholar
[48]

Yang, F.; Skripka, A.; Tabatabaei, M. S.; Hong, S. H.; Ren, F. Q.; Benayas, A.; Oh, J. K.; Martel, S.; Liu, X. Y.; Vetrone, F. et al. Multifunctional self-assembled supernanoparticles for deep-tissue bimodal imaging and amplified dual-mode heating treatment. ACS Nano 2019, 13, 408–420.
DOI Google Scholar
[49]

Martinac, B. The ion channels to cytoskeleton connection as potential mechanism of mechanosensitivity. Biochim. Biophys. Acta Biomembr. 2014, 1838, 682–691.
DOI Google Scholar
[50]

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.
DOI Google Scholar
[51]

Chen, R.; Romero, G.; Christiansen, M. G.; Mohr, A.; Anikeeva, P. Wireless magnetothermal deep brain stimulation. Science 2015, 347, 1477–1480.
DOI 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.
DOI Google Scholar
[53]

Lee, J. U.; Shin, W.; Lim, Y.; Kim, J.; Kim, W. R.; Kim, H.; Lee, J. H.; Cheon, J. Non-contact long-range magnetic stimulation of mechanosensitive ion channels in freely moving animals. Nat. Mater. 2021, 20, 1029–1036.
DOI Google Scholar
[54]

Nimpf, S.; Keays, D. A. Is magnetogenetics the new optogenetics. EMBO J. 2017, 36, 1643–1646.
DOI Google Scholar
[55]

Deng, W. L.; Zhou, Y. H.; Libanori, A.; Chen, G. R.; Yang, W. Q.; Chen, J. Piezoelectric nanogenerators for personalized healthcare. Chem. Soc. Rev. 2022, 51, 3380–3435.
DOI Google Scholar
[56]

Deng, W. L.; Libanori, A.; Xiao, X.; Fang, J.; Zhao, X.; Zhou, Y. H.; Chen, G. R.; Li, S.; Chen, J. Computational investigation of ultrasound induced electricity generation via a triboelectric nanogenerator. Nano Energy 2022, 91, 106656.
DOI Google Scholar
[57]

Zhou, Y. H.; Zhao, X.; Xu, J.; Fang, Y. S.; Chen, G. R.; Song, Y.; Li, S.; Chen, J. Giant magnetoelastic effect in soft systems for bioelectronics. Nat. Mater. 2021, 20, 1670–1676.
DOI Google Scholar
[58]

Yang, F.; Cui, H.; Wu, X.; Kim, S. J.; Hong, G. S. Ultrasound-activated luminescence with color tunability enabled by mechanoluminescent colloids and perovskite quantum dots. Nanoscale 2023, 15, 1629–1636.
DOI Google Scholar
[59]

Wang, W. L.; Wu, X.; Kevin Tang, K. W.; Pyatnitskiy, I.; Taniguchi, R.; Lin, P.; Zhou, R.; Capocyan, S. L. C.; Hong, G. S.; Wang, H. L. Ultrasound-triggered in situ photon emission for noninvasive optogenetics. J. Am. Chem. Soc. 2023, 145, 1097–1107.
DOI Google Scholar
[60]

Yang, F.; Wu, X.; Cui, H.; Jiang, S.; Ou, Z. H.; Cai, S.; Hong, G. S. Palette of rechargeable mechanoluminescent fluids produced by a biomineral-inspired suppressed dissolution approach. J. Am. Chem. Soc. 2022, 144, 18406–18418.
DOI Google Scholar
[61]

Yang, F.; Wu, X.; Cui, H.; Ou, Z. H.; Jiang, S.; Cai, S.; Zhou, Q.; Wong, B. G.; Huang, H.; Hong, G. S. A biomineral-inspired approach of synthesizing colloidal persistent phosphors as a multicolor, intravital light source. Sci. Adv. 2022, 8, eabo6743.
DOI Google Scholar
[62]

Yoo, J. W.; Chambers, E.; Mitragotri, S. Factors that control the circulation time of nanoparticles in blood: Challenges, solutions and future prospects. Curr. Pharm. Des. 2010, 16, 2298–2307.
DOI Google Scholar
[63]

Wu, X.; Zhu, X. J.; Chong, P.; Liu, J. L.; Andre, L. N.; Ong, K. S.; Brinson, K.; Mahdi, A. I.; Li, J. C.; Fenno, L. E. et al. Sono-optogenetics facilitated by a circulation-delivered rechargeable light source for minimally invasive optogenetics. Proc. Natl. Acad. Sci. USA 2019, 116, 26332–26342.
DOI Google Scholar
[64]

Zhang, Y. Y.; Zhang, X.; Wang, H. J.; Tian, Y.; Pan, H. Z.; Zhang, L. L.; Wang, F.; Chang, J. Remote regulation of optogenetic proteins by a magneto-luminescence microdevice. Adv. Funct. Mater. 2021, 31, 2006357.
DOI Google Scholar
[65]

Jiang, Y. W.; Parameswaran, R.; Li, X. J.; Carvalho-De-Souza, J. L.; Gao, X.; Meng, L. Y.; Bezanilla, F.; Shepherd, G. M. G.; Tian, B. Z. Nongenetic optical neuromodulation with silicon-based materials. Nat. Protoc. 2019, 14, 1339–1376.
DOI Google Scholar
[66]

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.
DOI Google Scholar
[67]

Jiang, Y. W.; Li, X. J.; Liu, B.; Yi, J.; Fang, Y.; Shi, F. Y.; Gao, X.; Sudzilovsky, E.; Parameswaran, R.; Koehler, K. et al. Rational design of silicon structures for optically controlled multiscale biointerfaces. Nat. Biomed. Eng. 2018, 2, 508–521.
DOI Google Scholar
[68]

Huang, Y. X.; Cui, Y. T.; Deng, H. J.; Wang, J. J.; Hong, R. Q.; Hu, S. H.; Hou, H. Q.; Dong, Y. R.; Wang, H. C.; Chen, J. Y. et al. Bioresorbable thin-film silicon diodes for the optoelectronic excitation and inhibition of neural activities. Nat. Biomed. Eng. 2023, 7, 486–498.
DOI Google Scholar
[69]

Zhu, M. T.; Nie, G. J.; Meng, H.; Xia, T.; Nel, A.; Zhao, Y. L. Physicochemical properties determine nanomaterial cellular uptake, transport, and fate. Acc. Chem. Res. 2013, 46, 622–631.
DOI Google Scholar
[70]

Zheng, W.; Huang, P.; Tu, D. T.; Ma, E.; Zhu, H. M.; Chen, X. Y. Lanthanide-doped upconversion nano-bioprobes: Electronic structures, optical properties, and biodetection. Chem. Soc. Rev. 2015, 44, 1379–1415.
DOI Google Scholar
[71]

Hong, G. S. Seeing the sound. Science 2020, 369, 638–638.
DOI Google Scholar
Publication history
Copyright
Acknowledgements

Publication history

Received: 29 June 2023
Revised: 26 August 2023
Accepted: 28 August 2023
Published: 03 October 2023
Issue date: February 2024

Copyright

© Tsinghua University Press 2023

Acknowledgements

G. S. H. acknowledges the Rita Allen Foundation Scholars Award, the Beckman Technology Development Grant, the grant from the focused ultrasound (FUS) Foundation, the gift from the Spinal Muscular Atrophy (SMA) Foundation, the gift from the Pinetops Foundation, two seed grants from the Wu Tsai Neurosciences Institute, and two seed grants from the Bio-X Initiative of Stanford University. X. W. acknowledges the support by the Stanford Graduate Fellowship.

Return