AI Chat Paper
Discover the SciOpen Platform and Achieve Your Research Goals with Ease.
Search articles, authors, keywords, DOl and etc.
{{expandStatus?'Exit ':''}}Advanced Search
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.
Won, S. M.; Song, E. M.; Reeder, J. T.; Rogers, J. A. Emerging modalities and implantable technologies for neuromodulation. Cell 2020, 181, 115–135.
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.
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.
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.
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.
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.
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.
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.
Hong, G. S.; Antaris, A. L.; Dai, H. J. Near-infrared fluorophores for biomedical imaging. Nat. Biomed. Eng. 2017, 1, 0010.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Li, J. C.; Pu, K. Y. Semiconducting polymer nanomaterials as near-infrared photoactivatable protherapeutics for cancer. Acc. Chem. Res. 2020, 53, 752–762.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Martinac, B. The ion channels to cytoskeleton connection as potential mechanism of mechanosensitivity. Biochim. Biophys. Acta Biomembr. 2014, 1838, 682–691.
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.
Chen, R.; Romero, G.; Christiansen, M. G.; Mohr, A.; Anikeeva, P. Wireless magnetothermal deep brain stimulation. Science 2015, 347, 1477–1480.
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.
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.
Nimpf, S.; Keays, D. A. Is magnetogenetics the new optogenetics. EMBO J. 2017, 36, 1643–1646.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hong, G. S. Seeing the sound. Science 2020, 369, 638–638.
1207
Views
182
Downloads
6
Crossref
6
Web of Science
6
Scopus
0
CSCD
Altmetrics
京公网安备11010802044758号