Materials for flexible bioelectronic systems as chronic neural interfaces.
Journal
Nature materials
ISSN: 1476-4660
Titre abrégé: Nat Mater
Pays: England
ID NLM: 101155473
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
14
11
2019
accepted:
09
04
2020
entrez:
29
5
2020
pubmed:
29
5
2020
medline:
25
11
2020
Statut:
ppublish
Résumé
Engineered systems that can serve as chronically stable, high-performance electronic recording and stimulation interfaces to the brain and other parts of the nervous system, with cellular-level resolution across macroscopic areas, are of broad interest to the neuroscience and biomedical communities. Challenges remain in the development of biocompatible materials and the design of flexible implants for these purposes, where ulimate goals are for performance attributes approaching those of conventional wafer-based technologies and for operational timescales reaching the human lifespan. This Review summarizes recent advances in this field, with emphasis on active and passive constituent materials, design architectures and integration methods that support necessary levels of biocompatibility, electronic functionality, long-term stable operation in biofluids and reliability for use in vivo. Bioelectronic systems that enable multiplexed electrophysiological mapping across large areas at high spatiotemporal resolution are surveyed, with a particular focus on those with proven chronic stability in live animal models and scalability to thousands of channels over human-brain-scale dimensions. Research in materials science will continue to underpin progress in this field of study.
Identifiants
pubmed: 32461684
doi: 10.1038/s41563-020-0679-7
pii: 10.1038/s41563-020-0679-7
doi:
Substances chimiques
Biocompatible Materials
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
590-603Références
Fang, J. Y. & Tolleson, C. The role of deep brain stimulation in Parkinson’s disease: an overview and update on new developments. Neuropsychiatr. Dis. Treat 13, 723–732 (2017).
doi: 10.2147/NDT.S113998
Wellman, S. M. et al. A materials roadmap to functional neural interface design. Adv. Funct. Mater. 28, 1701269 (2018).
doi: 10.1002/adfm.201701269
Fu, T. M., Hong, G., Viveros, R. D., Zhou, T. & Lieber, C. M. Highly scalable multichannel mesh electronics for stable chronic brain electrophysiology. Proc. Natl Acad. Sci. USA 114, E10046–E10055 (2017).
doi: 10.1073/pnas.1717695114
Rivnay, J., Wang, H., Fenno, L., Delsseroth, K. & Mallaras, G. G. Next-generation probes, particles, and proteins for neural interfacing. Sci. Adv. 3, e1601649 (2017).
doi: 10.1126/sciadv.1601649
Berényi, A. et al. Large-scale, high-density (up to 512 channels. recording of local circuits in behaving animals). J. Neurophysiol. 111, 1132–1149 (2014).
doi: 10.1152/jn.00785.2013
Robinson, J. T. et al. Vertical nanowire electrode arrays as a scalable platform for intracellular interfacing to neuronal circuits. Nat. Nanotechnol. 7, 180–184 (2012).
doi: 10.1038/nnano.2011.249
Ershad, F., Sim, K., Thukral, A., Zhang, Y. S. & Yu, C. Invited article: emerging soft bioelectronics for cardiac health diagnosis and treatment. APL Mater. 7, 031301 (2019).
doi: 10.1063/1.5060270
Gassert, R. & Dietz, V. Rehabilitation robots for the treatment of sensorimotor deficits: a neurophysiological perspective. J. Neuroeng. Rehabil. 15, 46 (2018).
doi: 10.1186/s12984-018-0383-x
Sanders, R. S. & Lee, M. T. Implantable pacemakers. Proc. IEEE 84, 480–486 (1996).
doi: 10.1109/5.486749
Mayberg, H. S. et al. Deep brain stimulation for treatment-resistant depression. Neuron 45, 651–660 (2005).
doi: 10.1016/j.neuron.2005.02.014
Rousche, P. J. & Normann, R. A. Chronic recording capability of the Utah intracortical electrode array in cat sensory cortex. J. Neurosci. Methods 82, 1–15 (1998).
doi: 10.1016/S0165-0270(98)00031-4
Hiremath, S. V. et al. Human perception of electrical stimulation on the surface of somatosensory cortex. PLoS ONE 12, e0176020 (2017).
doi: 10.1371/journal.pone.0176020
Vetter, R. J., Williams, J. C., Hetke, J. F., Nunamaker, E. A. & Kipke, D. R. Chronic neural recording using silicon-substrate microelectrode arrays implanted in cerebral cortex. IEEE Trans. Biomed. Eng. 51, 896–904 (2004).
doi: 10.1109/TBME.2004.826680
Wark, H. A. C. et al. A new high-density (25 electrodes/mm
doi: 10.1088/1741-2560/10/4/045003
Bouton, C. E. et al. Restoring cortical control of functional movement in a human with quadriplegia. Nature 533, 247–250 (2016).
doi: 10.1038/nature17435
Pandarinath, C. et al. High performance communication by people with paralysis using an intracortical brain–computer interface. eLife 6, e18554 (2017).
doi: 10.7554/eLife.18554
Bai, Q., Wise, K. D. & Anderson, D. J. A high-yield microassembly structure for three-dimensional microelectrode arrays. IEEE Trans. Biomed. Eng. 47, 281–289 (2000).
doi: 10.1109/10.827288
Dai, X., Zhou, W., Gao, T., Liu, J. & Lieber, C. M. Three-dimensional mapping and regulation of action potential propagation in nanoelectronics innervated tissues. Nat. Nanotechnol. 11, 776–782 (2016).
doi: 10.1038/nnano.2016.96
Montgomery, K. L. et al. Wirelessly powered, fully internal optogenetics for brain, spinal and peripheral circuits in mice. Nat. Methods 12, 969–974 (2015).
doi: 10.1038/nmeth.3536
Canales, A. et al. Multifunctional fibers for simultaneous optical, electrical and chemical interrogation of neural circuits in vivo. Nat. Biotechnol. 33, 277–284 (2015).
doi: 10.1038/nbt.3093
Viventi, J. et al. A conformal, bio-interfaced class of silicon electronics for mapping cardiac electrophysiology. Sci. Transl. Med. 2, 24ra22 (2010).
doi: 10.1126/scitranslmed.3000738
Viventi, J. et al. Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo. Nat. Neurosci. 14, 1599–1605 (2011).
doi: 10.1038/nn.2973
Minev, I. R. et al. Electronic dura mater for long-term multimodal neural interfaces. Science 347, 159–163 (2015).
doi: 10.1126/science.1260318
Tian, B. et al. Three-dimensional, flexible nanoscale field-effect transistors as localized bioprobes. Science 329, 830–834 (2010).
doi: 10.1126/science.1192033
Khodagholy, D. et al. Organic electronics for high-resolution electrocorticography of the human brain. Sci. Adv. 2, e1601027 (2016).
doi: 10.1126/sciadv.1601027
Park, J.-S., Chae, H., Chung, H. K. & Lee, S. I. Thin film encapsulation for flexible AM-OLED: a review. Semicond. Sci. Technol. 26, 034001 (2011).
doi: 10.1088/0268-1242/26/3/034001
Xie, X., Ritch, L., Mcrugu, S., Tathircddy, P. & Solzbacher, F. Plasma-assisted atomic layer deposition of Al
doi: 10.1063/1.4748322
Luan, L. et al. Ultraflexible nanoelectronic probes form reliable, glial scar-free neural integration. Sci. Adv. 3, e1601966 (2017).
doi: 10.1126/sciadv.1601966
Musk, E. An integrated brain–machine interface platform with thousands of channels. J. Med. Internet. Res 21, e16194 (2019).
McCallum, G. A. et al. Chronic interfacing with the autonomic nervous system using carbon nanotube (CNT) yarn electrodes. Sci. Rep. 7, 11723 (2017).
doi: 10.1038/s41598-017-10639-w
Yang, X. et al. Bioinspired neuron-like electronics. Nat. Mater. 18, 510–517 (2019).
doi: 10.1038/s41563-019-0292-9
Kozai, T. D. Y. et al. Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat. Mater. 11, 1065–1073 (2012).
doi: 10.1038/nmat3468
Wang, L. et al. Ultrasoft and highly stretchable hydrogel optical fibers for in vivo optogenetic modulations. Adv. Opt. Mater. 6, 1800427 (2018).
doi: 10.1002/adom.201800427
Khodagholy, D. et al. NeuroGrid: recording action potentials from the surface of the brain. Nat. Neurosci. 18, 310–315 (2015).
doi: 10.1038/nn.3905
Lee, W. et al. Nonthrombogenic, stretchable, active multielectrode array for electroanatomical mapping. Sci. Adv. 4, eaau2426 (2018).
doi: 10.1126/sciadv.aau2426
Campana, A. et al. Electrocardiographic recording with conformable organic electrochemical transistor fabricated on resorbable bioscaffold. Adv. Mater. 26, 3874–3878 (2014).
doi: 10.1002/adma.201400263
Zhang, Y. C. et al. Climbing-inspired twining electrodes using shape memory for peripheral nerve stimulation and recording. Sci. Adv. 5, eaaw1066 (2019).
doi: 10.1126/sciadv.aaw1066
Borschel, G. H., Kia, K. F., Kuzon, W. M. Jr & Dennis, R. G. Mechanical properties of acellular peripheral nerve. J. Surg. Res. 114, 133–139 (2003).
doi: 10.1016/S0022-4804(03)00255-5
Kim, D.-H. et al. Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics. Nat. Mater. 9, 511–517 (2012).
doi: 10.1038/nmat2745
Liu, J. et al. Syringe-injectable electronics. Nat. Nanotechnol. 10, 629–636 (2015).
doi: 10.1038/nnano.2015.115
Yan, Z. et al. Three-dimensional mesostructures as high-temperature growth templates, electronic cellular scaffolds, and self-propelled microrobots. Proc. Natl Acad. Sci. USA 114, E9455–E9464 (2017).
doi: 10.1073/pnas.1713805114
Bhunia, S., Majerus, S. & Sawan, M. Implantable Biomedical Microsystems: Design Principles and Applications (Elsevier, 2015).
Johnson, L. A. et al. Direct electrical stimulation of the somatosensory cortex in humans using electrocorticography electrodes: a qualitative and quantitative report. J. Neural. Eng. 10, 036021 (2013).
doi: 10.1088/1741-2560/10/3/036021
Waziri, A. et al. Initial surgical experience with a dense cortical microarray in epileptic patients undergoing craniotomy for subdural electrode implantation. Neurosurgery 64, 540–545 (2009).
doi: 10.1227/01.NEU.0000337575.63861.10
Khodagholy, D. et al. In vivo recordings of brain activity using organic transistors. Nat. Commun. 4, 1575 (2013).
doi: 10.1038/ncomms2573
Kaltenbrunner, M. et al. An ultra-lightweight design for imperceptible plastic electronics. Nature 499, 458–463 (2013).
doi: 10.1038/nature12314
Jun, J. J. et al. Fully integrated silicon probes for high-density recording of neural activity. Nature 551, 232–236 (2017).
doi: 10.1038/nature24636
Lopez, C. M. et al. An implantable 455-active-electrode 52-channel CMOS neural probe. IEEE J. Solid-State Circuits 49, 248–261 (2014).
doi: 10.1109/JSSC.2013.2284347
Tian, B. et al. Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. Nat. Mater. 11, 986–994 (2012).
doi: 10.1038/nmat3404
Xie, C. et al. Three-dimensional macroporous nanoelectronic networks as minimally invasive brain probes. Nat. Mater. 14, 1286–1293 (2015).
doi: 10.1038/nmat4427
Patel, S. R. & Lieber, C. M. Precision electronic medicine in the brain. Nat. Biotechnol. 37, 1007–1012 (2019).
doi: 10.1038/s41587-019-0234-8
Escabi, M. A. et al. A high-density, high-channel count, multiplexed mu ECoG array for auditory-cortex recordings. J. Neurophysiol. 112, 1566–1583 (2014).
doi: 10.1152/jn.00179.2013
Hwang, G.-T. et al. In vivo silicon-based flexible radio frequency integrated circuits monolithically encapsulated with biocompatible liquid crystal polymers. ACS Nano 7, 4545–4553 (2013).
doi: 10.1021/nn401246y
Sim, K., Rao, Z., Li, Y., Yang, D. & Yu, C. Curvy surface conformal ultra-thin transfer printed Si optoelectronic penetrating microprobe arrays. npj Flex. Electron 2, 2 (2018).
Paetzold, R., Winnacker, A., Henseler, D., Cesari, V. & Heuser, K. Permeation rate measurements by electrical analysis of calcium corrosion. Rev. Sci. Instrum. 74, 5147–5150 (2003).
doi: 10.1063/1.1626015
Choi, M.-C., Kim, Y. & Ha, C.-S. Polymers for flexible displays: from material selection to device applications. Prog. Polym. Sci. 33, 581–630 (2008).
doi: 10.1016/j.progpolymsci.2007.11.004
Debeaufort, F., Voilley, A. & Meares, P. Water vapor permeability and diffusivity through methylcelluloseedible films. J. Membrane. Sci. 91, 125–133 (1994).
doi: 10.1016/0376-7388(94)00024-7
Ahmad, J., Bazaka, K., Anderson, L. J., White, R. D. & Jacob, M. V. Materials and methods for encapsulation of OPV: a review. Renew. Sustain. Energy Rev 27, 104–117 (2013).
doi: 10.1016/j.rser.2013.06.027
McKeen, L. W. Permeability Properties of Plastics and Elastomers (Elsevier, 2016).
Groner, M. D., George, S. M., McLean, R. S. & Carcia, P. F. Gas diffusion barriers on polymers using Al
doi: 10.1063/1.2168489
Yasuda, H. & Stannett, V. Permeation, solution, and diffusion of water in some high polymers. J. Polym. Sci. 57, 907–923 (1962).
doi: 10.1002/pol.1962.1205716571
Feng, J., Berger, K. R. & Douglas, E. P. Water vapor transport in liquid crystalline and non-liquid crystalline epoxies. J. Mater. Sci. 39, 3413–3423 (2004).
doi: 10.1023/B:JMSC.0000026944.85440.f3
Barrie, J. A. & Machin, D. The sorption and diffusion of water in silicone rubbers. Part II. Filled rubbers. J. Macromol. Sci. B 3, 673–692 (1969).
doi: 10.1080/00222346908217113
Davis, E. M., Benetators, N. M., Regnault, W. F., Winey, K. I. & Elabd, Y. A. The influence of thermal history on structure and water transport in parylene C coatings. Polymer 52, 5378–5386 (2011).
doi: 10.1016/j.polymer.2011.08.010
Seo, S.-W. et al. Moisture permeation through ultrathin TiO
doi: 10.1143/APEX.5.035701
Nagai, S. Approximation of effective moisture-diffusion coefficient to characterize performance of a barrier coating. J. Appl. Phys. 114, 174302 (2013).
doi: 10.1063/1.4828872
Yu, D., Yang, Y.-Q., Chen, Z., Tao, Y. & Liu, Y.-F. Recent progress on thin-film encapsulation technologies for organic electronic devices. Opt. Commun. 362, 43–49 (2016).
doi: 10.1016/j.optcom.2015.08.021
Meyer, J. et al. Al
doi: 10.1002/adma.200803440
Fang, H. et al. Capacitively coupled arrays of multiplexed flexible silicon transistors for long-term cardiac electrophysiology. Nat. Biomed. Eng. 1, 0038 (2017).
doi: 10.1038/s41551-017-0038
Lopez, C. M. 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. 11, 510–522 (2017).
doi: 10.1109/TBCAS.2016.2646901
Song, E., Li, J. & Rogers, J. A. Barrier materials for flexible bioelectronic implants with chronic stability-current approaches and future directions. APL Mater. 7, 050902 (2019).
doi: 10.1063/1.5094415
Oehler, A. & Tomozawa, M. Water diffusion into silica glass at a low temperature under high water vapor pressure. J. Non. Cryst. Solids 347, 211–219 (2004).
doi: 10.1016/j.jnoncrysol.2004.07.013
Lin, Y., Tsui, T. Y. & Vlassak, J. J. Water diffusion and fracture in organosilicate galss film stacks. Acta Mater. 55, 2455–2464 (2007).
doi: 10.1016/j.actamat.2006.11.040
Fang, H. et al. Ultrathin, transferred layers of thermally grown silicon dioxide as biofluid barriers for biointegrated flexible electronic systems. Proc. Natl Acad. Sci. USA 113, 11682–11687 (2016).
doi: 10.1073/pnas.1605269113
Song, E. et al. Thin, transferred layers of silicon dioxide and silicon nitride as water and ion barriers for implantable flexible electronic systems. Adv. Electron. Mater. 3, 1700077 (2017).
doi: 10.1002/aelm.201700077
Song, E. et al. Ultrathin trilayer assemblies as long-lived barriers against water and ion penetration in flexible bioelectronic systems. ACS Nano 12, 10317–10326 (2018).
doi: 10.1021/acsnano.8b05552
Li, J. et al. Conductively coupled flexible silicon electronic systems for chronic neural electrophysiology. Proc. Natl Acad. Sci. USA 115, E9542–E9549 (2018).
doi: 10.1073/pnas.1813187115
Lee, Y. K. et al. Dissolution of monocrystalline silicon nanomembranes and their use as encapsulation layers and electrical interfaces in water-soluble electronics. ACS Nano 11, 12562–12572 (2017).
doi: 10.1021/acsnano.7b06697
Li, J. et al. Ultrathin, transferred layers of metal silicide as faradaic electrical interfaces and biofluid barriers for flexible bioelectronic implants. ACS Nano 13, 660–670 (2019).
doi: 10.1021/acsnano.8b07806
Cogan, S. F., Edell, D. J., Guzelian, A. A., Liu, Y. P. & Edell, R. Plasma-enhanced chemical vapor deposited silicon carbide as an implantable dielectric coating. J. Biomed. Mater. Res. A 67a, 856–867 (2003).
doi: 10.1002/jbm.a.10152
Knaack, G. L. et al. In vivo characterization of amorphous silicon carbide as a biomaterial for chronic neural interfaces. Front. Neurosci. 10, 301 (2016).
doi: 10.3389/fnins.2016.00301
Lei, X. et al. SiC protective coating for photovoltaic retinal prosthesis. J. Neural. Eng 13, 046016 (2016).
Phan, H.-P. et al. Long-lived, transferred crystalline silicon carbide nanomembranes for implantable flexible electronics. ACS Nano 13, 11572–11581 (2019).
doi: 10.1021/acsnano.9b05168
Hollenberg, B. A., Richards, C. D., Richards, R., Bahr, D. F. & Rector, D. M. A MEMS fabricated flexible electrode array for recording surface field potentials. J. Neurosci. Methods 153, 147–153 (2006).
doi: 10.1016/j.jneumeth.2005.10.016
Benison, A. M., Rector, D. M. & Barth, D. S. Hemispheric mapping of secondary somatosensory cortex in the rat. J. Neurophysiol. 97, 200–207 (2007).
doi: 10.1152/jn.00673.2006
Molina-Luna, K. et al. Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays. J. Neurosci. Methods 161, 118–125 (2007).
doi: 10.1016/j.jneumeth.2006.10.025
Kim, J., Wilson, J. A. & Williams, J. C. A cortical recording platform utilizing μECoG electrode arrays. In 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society 5353–5357 (IEEE, 2007).
Rubehn, B., Bosman, C., Oostenveld, R., Fries, P. & Stieglitz, T. A MEMS-based flexible multichannel ECoG-electrode array. J. Neural Eng. 6, 036003 (2009).
doi: 10.1088/1741-2560/6/3/036003
Ledochowitsch, P. et al. Fabrication and testing of a large area, high density, parylene MEMS µECoG array. In 2011 IEEE 24th International Conference on Micro Electro Mechanical Systems 1031–1034 (IEEE, 2011).
Besle, J. et al. Tuning of the human neocortex to the temporal dynamics of attended events. J. Neurosci. 31, 3176–3185 (2011).
doi: 10.1523/JNEUROSCI.4518-10.2011
Pasley, B. N. et al. Reconstructing speech from human auditory cortex. PLoS Biol. 10, e1001251 (2012).
doi: 10.1371/journal.pbio.1001251
Hotson, G. et al. Individual finger control of a modular prosthetic limb using high-density electrocorticography in a human subject. J. Neural Eng. 13, 026017 (2016).
doi: 10.1088/1741-2560/13/2/026017
Kellis, S. et al. Multi-scale analysis of neural activity in humans: implications for micro-scale electrocorticography. Clin. Neurophysiol. 127, 591–601 (2016).
doi: 10.1016/j.clinph.2015.06.002
Kaiju, T. et al. High spatiotemporal resolution ECoG recording of somatosensory evoked potentials with flexible micro-electrode arrays. Front. Neural Circuits 11, 20 (2017).
doi: 10.3389/fncir.2017.00020
Chiang, C.-H. et al. The neural matrix: kiloscale neural interfaces for long-term recording. Sci. Transl. Med. 12, eaay4682 (2020).
doi: 10.1126/scitranslmed.aay4682
Song, E. et al. Flexible electronic/optoelectronic microsystems with scalable designs for chronic biointegration. Proc. Natl Acad. Sci. USA 116, 15398–15406 (2019).
doi: 10.1073/pnas.1907697116
Lee, W. et al. Transparent, conformable, active multielectrode array using organic electrochemical transistors. Proc. Natl Acad. Sci. USA 114, 10554–10559 (2017).
doi: 10.1073/pnas.1703886114
Yu, K. J. et al. Bioresorbable silicon electronics for transient spatiotemporal mapping of electrical activity from the cerebral cortex. Nat. Mater. 15, 782–791 (2016).
doi: 10.1038/nmat4624