Ultra-Sharp Nanowire Arrays Natively Permeate, Record, and Stimulate Intracellular Activity in Neuronal and Cardiac Networks

Liu, Ren; Lee, Jihwan; Tchoe, Youngbin; Robin, Gaelle; Bourhis, Andrew; D'Antonio-Chronowska, Agnieszka; Pre, Deborah; Lee, Sang Heon; Ro, Yun Goo; Vatsyayan, Ritwik; Tonsfeldt, Karen; Hossain, Lorraine A.; Phipps, Mary Elizabeth; Yoo, Jinkyoung; Nogan, John; Martinez, Jennifer S.; Frazer, Kelly; Bang, Anne; Dayeh, Shadi A.

doi:10.1002/adfm.202108378

Ultra-Sharp Nanowire Arrays Natively Permeate, Record, and Stimulate Intracellular Activity in Neuronal and Cardiac Networks

Journal Article · Sat Nov 06 00:00:00 EDT 2021 · Advanced Functional Materials

DOI:https://doi.org/10.1002/adfm.202108378· OSTI ID:1832378

Liu, Ren ^[1]; Lee, Jihwan ^[1]; Tchoe, Youngbin ^[1]; Robin, Gaelle ^[2]; Bourhis, Andrew ^[1]; D'Antonio-Chronowska, Agnieszka ^[1]; Pre, Deborah ^[2]; Lee, Sang Heon ^[1]; Ro, Yun Goo ^[1]; Vatsyayan, Ritwik ^[1]; Tonsfeldt, Karen ^[1]; Hossain, Lorraine A. ^[1]; Phipps, Mary Elizabeth ^[3]; ^[3]; Nogan, John ^[4]; Martinez, Jennifer S. ^[5]; Frazer, Kelly ^[1]; Bang, Anne ^[2]; ^[1]

Univ. of California, San Diego, CA (United States)
Sanford-Burnham Medical Research Institute, La Jolla, CA (United States)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Northern Arizona Univ., Flagstaff, AZ (United States)

Intracellular access with high spatiotemporal resolution can enhance the understanding of how neurons or cardiomyocytes regulate and orchestrate network activity and how this activity can be affected with pharmacology or other interventional modalities. Nanoscale devices often employ electroporation to transiently permeate the cell membrane and record intracellular potentials, which tend to decrease rapidly with time. Here, one reports innovative scalable, vertical, ultrasharp nanowire arrays that are individually addressable to enable long-term, native recordings of intracellular potentials. One reports electrophysiological recordings that are indicative of intracellular access from 3D tissue-like networks of neurons and cardiomyocytes across recording days and that do not decrease to extracellular amplitudes for the duration of the recording of several minutes. The findings are validated with cross-sectional microscopy, pharmacology, and electrical interventions. The experiments and simulations demonstrate that the individual electrical addressability of nanowires is necessary for high-fidelity intracellular electrophysiological recordings. This work advances the understanding of and control over high-quality multichannel intracellular recordings and paves the way toward predictive, high-throughput, and low-cost electrophysiological drug screening platforms.

View Accepted Manuscript (DOE)

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); USDOE; USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: 89233218CNA000001; AC04-94AL85000

OSTI ID:: 1832378

Alternate ID(s):: OSTI ID: 1830257

Report Number(s):: LA-UR--21-21277

Journal Information:: Advanced Functional Materials, Journal Name: Advanced Functional Materials Journal Issue: 8 Vol. 32; ISSN 1616-301X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (53)

Development and Translation of PEDOT:PSS Microelectrodes for Intraoperative Monitoring Ganji, Mehran; Kaestner, Erik; Hermiz, John Advanced Functional Materials, Vol. 28, Issue 12 https://doi.org/10.1002/adfm.201700232	journal	May 2017
The extracellular patch clamp: A method for resolving currents through individual open channels in biological membranes Neher, Erwin; Sakmann, Bert; Steinbach, Joe Henry Pfl�gers Archiv European Journal of Physiology, Vol. 375, Issue 2 https://doi.org/10.1007/BF00584247	journal	July 1978
Action potential threshold of hippocampal pyramidal cells in vivo is increased by recent spiking activity Henze, D. A.; Buzsáki, G. Neuroscience, Vol. 105, Issue 1 https://doi.org/10.1016/S0306-4522(01)00167-1	journal	July 2001
Neurite outgrowth and synaptophysin expression of postnatal CNS neurons on GaP nanowire arrays in long-term retinal cell culture Piret, Gaëlle; Perez, Maria-Thereza; Prinz, Christelle N. Biomaterials, Vol. 34, Issue 4 https://doi.org/10.1016/j.biomaterials.2012.10.042	journal	January 2013
Size-dependent long-term tissue response to biostable nanowires in the brain Gällentoft, Lina; Pettersson, Lina M. E.; Danielsen, Nils Biomaterials, Vol. 42 https://doi.org/10.1016/j.biomaterials.2014.11.051	journal	February 2015
Microscale dynamics of electrophysiological markers of epilepsy Yang, Jimmy C.; Paulk, Angelique C.; Salami, Pariya Clinical Neurophysiology, Vol. 132, Issue 11 https://doi.org/10.1016/j.clinph.2021.06.024	journal	November 2021
Advances in three-dimensional nanostructures for intracellular recordings from electrogenic cells Khraiche, Massoud L.; El Hassan, Rima Journal of Science: Advanced Materials and Devices, Vol. 5, Issue 3 https://doi.org/10.1016/j.jsamd.2020.07.003	journal	September 2020
Influence of nanoscale surface roughness on neural cell attachment on silicon Khan, Saida P.; Auner, Gregory G.; Newaz, Golam M. Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 1, Issue 2 https://doi.org/10.1016/j.nano.2005.03.007	journal	June 2005
Sub-millimeter ECoG pitch in human enables higher fidelity cognitive neural state estimation Hermiz, John; Rogers, Nicholas; Kaestner, Erik NeuroImage, Vol. 176 https://doi.org/10.1016/j.neuroimage.2018.04.027	journal	August 2018
A Human iPSC Double-Reporter System Enables Purification of Cardiac Lineage Subpopulations with Distinct Function and Drug Response Profiles Zhang, Joe Z.; Termglinchan, Vittavat; Shao, Ning-Yi Cell Stem Cell, Vol. 24, Issue 5 https://doi.org/10.1016/j.stem.2019.02.015	journal	May 2019
Association of Human iPSC Gene Signatures and X Chromosome Dosage with Two Distinct Cardiac Differentiation Trajectories D'Antonio-Chronowska, Agnieszka; Donovan, Margaret K. R.; Young Greenwald, William W. Stem Cell Reports, Vol. 13, Issue 5 https://doi.org/10.1016/j.stemcr.2019.09.011	journal	November 2019
The Role of Membrane Curvature in Nanoscale Topography-Induced Intracellular Signaling Lou, Hsin-Ya; Zhao, Wenting; Zeng, Yongpeng Accounts of Chemical Research, Vol. 51, Issue 5 https://doi.org/10.1021/acs.accounts.7b00594	journal	April 2018
Spontaneous Internalization of Cell Penetrating Peptide-Modified Nanowires into Primary Neurons Lee, Jae-Hyun; Zhang, Anqi; You, Siheng Sean Nano Letters, Vol. 16, Issue 2 https://doi.org/10.1021/acs.nanolett.6b00020	journal	January 2016
High Density Individually Addressable Nanowire Arrays Record Intracellular Activity from Primary Rodent and Human Stem Cell Derived Neurons Liu, Ren; Chen, Renjie; Elthakeb, Ahmed T. Nano Letters, Vol. 17, Issue 5 https://doi.org/10.1021/acs.nanolett.6b04752	journal	April 2017
Intracellular and Extracellular Recording of Spontaneous Action Potentials in Mammalian Neurons and Cardiac Cells with 3D Plasmonic Nanoelectrodes Dipalo, Michele; Amin, Hayder; Lovato, Laura Nano Letters, Vol. 17, Issue 6 https://doi.org/10.1021/acs.nanolett.7b01523	journal	May 2017
Intracellular Recording of Cardiomyocyte Action Potentials with Nanopatterned Volcano-Shaped Microelectrode Arrays Desbiolles, B. X. E.; de Coulon, E.; Bertsch, A. Nano Letters, Vol. 19, Issue 9 https://doi.org/10.1021/acs.nanolett.9b02209	journal	August 2019
Selective Formation of Porous Pt Nanorods for Highly Electrochemically Efficient Neural Electrode Interfaces Ganji, Mehran; Paulk, Angelique C.; Yang, Jimmy C. Nano Letters, Vol. 19, Issue 9 https://doi.org/10.1021/acs.nanolett.9b02296	journal	August 2019
Cell Membrane Disruption by Vertical Micro-/Nanopillars: Role of Membrane Bending and Traction Forces Capozza, Rosario; Caprettini, Valeria; Gonano, Carlo A. ACS Applied Materials & Interfaces, Vol. 10, Issue 34 https://doi.org/10.1021/acsami.8b08218	journal	August 2018
Tuning InAs Nanowire Density for HEK293 Cell Viability, Adhesion, and Morphology: Perspectives for Nanowire-Based Biosensors Bonde, Sara; Berthing, Trine; Madsen, Morten Hannibal ACS Applied Materials & Interfaces, Vol. 5, Issue 21 https://doi.org/10.1021/am402070k	journal	October 2013
Interfacing Silicon Nanowires with Mammalian Cells Kim, Woong; Ng, Jennifer K.; Kunitake, Miki E. Journal of the American Chemical Society, Vol. 129, Issue 23 https://doi.org/10.1021/ja071456k	journal	June 2007
Cell and Protein Compatibility of Parylene-C Surfaces Chang, Tracy Y.; Yadav, Vikramaditya G.; De Leo, Sarah Langmuir, Vol. 23, Issue 23 https://doi.org/10.1021/la7017049	journal	October 2007
Graphene and Nanowire Transistors for Cellular Interfaces and Electrical Recording Cohen-Karni, Tzahi; Qing, Quan; Li, Qiang Nano Letters, Vol. 10, Issue 3 https://doi.org/10.1021/nl1002608	journal	March 2010
Characterization of the Cell–Nanopillar Interface by Transmission Electron Microscopy Hanson, Lindsey; Lin, Ziliang Carter; Xie, Chong Nano Letters, Vol. 12, Issue 11 https://doi.org/10.1021/nl303163y	journal	October 2012
Mechanical Model of Vertical Nanowire Cell Penetration Xie, Xi; Xu, Alexander M.; Angle, Matthew R. Nano Letters, Vol. 13, Issue 12 https://doi.org/10.1021/nl403201a	journal	November 2013
In-cell recordings by extracellular microelectrodes Hai, Aviad; Shappir, Joseph; Spira, Micha E. Nature Methods, Vol. 7, Issue 3 https://doi.org/10.1038/nmeth.1420	journal	January 2010
Intracellular recordings of action potentials by an extracellular nanoscale field-effect transistor Duan, Xiaojie; Gao, Ruixuan; Xie, Ping Nature Nanotechnology, Vol. 7, Issue 3 https://doi.org/10.1038/nnano.2011.223	journal	December 2011
Vertical nanowire electrode arrays as a scalable platform for intracellular interfacing to neuronal circuits Robinson, Jacob T.; Jorgolli, Marsela; Shalek, Alex K. Nature Nanotechnology, Vol. 7, Issue 3 https://doi.org/10.1038/nnano.2011.249	journal	January 2012
Intracellular recording of action potentials by nanopillar electroporation Xie, Chong; Lin, Ziliang; Hanson, Lindsey Nature Nanotechnology, Vol. 7, Issue 3 https://doi.org/10.1038/nnano.2012.8	journal	February 2012
Free-standing kinked nanowire transistor probes for targeted intracellular recording in three dimensions Qing, Quan; Jiang, Zhe; Xu, Lin Nature Nanotechnology, Vol. 9, Issue 2 https://doi.org/10.1038/nnano.2013.273	journal	December 2013
The mechanobiology of brain function Tyler, William J. Nature Reviews Neuroscience, Vol. 13, Issue 12 https://doi.org/10.1038/nrn3383	journal	November 2012
Nanovolcano microelectrode arrays: toward long-term on-demand registration of transmembrane action potentials by controlled electroporation Desbiolles, Benoît X. E.; de Coulon, Etienne; Maïno, Nicolas Microsystems & Nanoengineering, Vol. 6, Issue 1 https://doi.org/10.1038/s41378-020-0178-7	journal	August 2020
A nanoelectrode array for obtaining intracellular recordings from thousands of connected neurons Abbott, Jeffrey; Ye, Tianyang; Krenek, Keith Nature Biomedical Engineering, Vol. 4, Issue 2 https://doi.org/10.1038/s41551-019-0455-7	journal	September 2019
Scalable ultrasmall three-dimensional nanowire transistor probes for intracellular recording Zhao, Yunlong; You, Siheng Sean; Zhang, Anqi Nature Nanotechnology, Vol. 14, Issue 8 https://doi.org/10.1038/s41565-019-0478-y	journal	July 2019
Tissue-specific extracellular matrix accelerates the formation of neural networks and communities in a neuron-glia co-culture on a multi-electrode array Lam, Doris; Enright, Heather A.; Cadena, Jose Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-40128-1	journal	March 2019
Evidence-based guidelines for controlling pH in mammalian live-cell culture systems Michl, Johanna; Park, Kyung Chan; Swietach, Pawel Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0393-7	journal	April 2019
Spatially confined responses of mouse visual cortex to intracortical magnetic stimulation from micro-coils Ryu, Sang Baek; Paulk, Angelique C.; Yang, Jimmy C. Journal of Neural Engineering, Vol. 17, Issue 5 https://doi.org/10.1088/1741-2552/abbd22	journal	October 2020
Microscale Physiological Events on the Human Cortical Surface Paulk, Angelique C.; Yang, Jimmy C.; Cleary, Daniel R. Cerebral Cortex, Vol. 31, Issue 8 https://doi.org/10.1093/cercor/bhab040	journal	March 2021
Spine-shaped gold protrusions improve the adherence and electrical coupling of neurons with the surface of micro-electronic devices Hai, Aviad; Dormann, Ada; Shappir, Joseph Journal of The Royal Society Interface, Vol. 6, Issue 41 https://doi.org/10.1098/rsif.2009.0087	journal	May 2009
Automatic objective thresholding to detect neuronal action potentials Tanskanen, Jarno M. A.; Kapucu, Fikret E.; Vornanen, Inkeri 2016 24th European Signal Processing Conference (EUSIPCO) https://doi.org/10.1109/EUSIPCO.2016.7760331	conference	August 2016
Monitoring pH, temperature and humidity in long-term stem cell culture in CO2 incubator Kattipparambil Rajan, Dhanesh; Verho, Jarmo; Kreutzer, Joose 2017 IEEE International Symposium on Medical Measurements and Applications (MeMeA) https://doi.org/10.1109/MeMeA.2017.7985922	conference	May 2017
On the threshold based neuronal spike detection, and an objective criterion for setting the threshold Tanskanen, Jarno M. A.; Kapucu, Fikret E.; Hyttinen, Jari A. K. 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER) https://doi.org/10.1109/NER.2015.7146799	conference	April 2015
Low-level Mechanisms for Processing Odor Information in the Behaving Animal Wachowiak, Matt; Wesson, Daniel W.; Pírez, Nicolás Annals of the New York Academy of Sciences, Vol. 1170, Issue 1 https://doi.org/10.1111/j.1749-6632.2009.04015.x	journal	July 2009
Intracellular action potential recordings from cardiomyocytes by ultrafast pulsed laser irradiation of fuzzy graphene microelectrodes Dipalo, Michele; Rastogi, Sahil K.; Matino, Laura Science Advances, Vol. 7, Issue 15 https://doi.org/10.1126/sciadv.abd5175	journal	April 2021
Detection, Stimulation, and Inhibition of Neuronal Signals with High-Density Nanowire Transistor Arrays Patolsky, Fernando; Timko, Brian P.; Yu, Guihua Science, Vol. 313, Issue 5790, p. 1100-1104 https://doi.org/10.1126/science.1128640	journal	August 2006
Distal Initiation and Active Propagation of Action Potentials in Interneuron Dendrites Martina, Marco; Vida, Imre; Jonas, Peter Science, Vol. 287, Issue 5451 https://doi.org/10.1126/science.287.5451.295	journal	January 2000
Natural Waking and Sleep States: A View From Inside Neocortical Neurons Steriade, M.; Timofeev, I.; Grenier, F. Journal of Neurophysiology, Vol. 85, Issue 5 https://doi.org/10.1152/jn.2001.85.5.1969	journal	May 2001
Correlation Structure in Micro-ECoG Recordings is Described by Spatially Coherent Components Rogers, Nicholas; Hermiz, John; Ganji, Mehran PLOS Computational Biology, Vol. 15, Issue 2 https://doi.org/10.1371/journal.pcbi.1006769	journal	February 2019
Maximum Diastolic Potential of Human Induced Pluripotent Stem Cell-Derived Cardiomyocytes Depends Critically on IKr Doss, Michael Xavier; Di Diego, José M.; Goodrow, Robert J. PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0040288	journal	July 2012
Positive feedback and synchronized bursts in neuronal cultures Huang, Yu-Ting; Chang, Yu-Lin; Chen, Chun-Chung PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0187276	journal	November 2017
Communication between Brain Areas Based on Nested Oscillations Bonnefond, Mathilde; Kastner, Sabine; Jensen, Ole eneuro, Vol. 4, Issue 2 https://doi.org/10.1523/ENEURO.0153-16.2017	journal	March 2017
Multisite Attenuated Intracellular Recordings by Extracellular Multielectrode Arrays, a Perspective Spira, Micha E.; Shmoel, Nava; Huang, Shun-Ho M. Frontiers in Neuroscience, Vol. 12 https://doi.org/10.3389/fnins.2018.00212	journal	April 2018
Cortical Network Synchrony Under Applied Electrical Field in vitro Tang-Schomer, Min D.; Jackvony, Taylor; Santaniello, Sabato Frontiers in Neuroscience, Vol. 12 https://doi.org/10.3389/fnins.2018.00630	journal	September 2018
Stimulus Driven Single Unit Activity From Micro-Electrocorticography Hermiz, John; Hossain, Lorraine; Arneodo, Ezequiel M. Frontiers in Neuroscience, Vol. 14 https://doi.org/10.3389/fnins.2020.00055	journal	February 2020

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