Three-dimensional fuzzy graphene ultra-microelectrodes for sub-cellular electrical recordings

Sahil K. Rastogi; Jacqueline Bliley; Laura Matino; Raghav Garg; Francesca Santoro; Adam W. Feinberg; Tzahi Cohen-Karni

doi:10.1007/s12274-020-2695-y

AI Chat Paper

Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.

Chat more with AI

| Sign up

Browse by Subject

Search for peer-reviewed journals with full access.

Journals A - Z

About Us

Discover the SciOpen Platform and Achieve Your Research Goals with Ease.

About Us

Publish with Us

Support

Search articles, authors, keywords, DOl and etc.

Published Date

Reset Search

{{expandStatus?'Exit ':''}}Advanced Search

Journals A - Z

About Us

Publish with Us

Support

Article Link

Cite

EndNote(RIS) BibTeX

Collect

Submit Manuscript

Show Outline

Outline

Show full outline

Hide outline

Outline

Show full outline

Hide outline

Research Article

Three-dimensional fuzzy graphene ultra-microelectrodes for sub-cellular electrical recordings

Sahil K. Rastogi^¹, Jacqueline Bliley^¹, Laura Matino^{²^,³}, Raghav Garg^⁴, Francesca Santoro^², Adam W. Feinberg^{¹^,⁴}, Tzahi Cohen-Karni^{¹^,⁴}(

)

1Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA, 15213, USA

2Center for Advanced Biomaterials for Healthcare, Istituto Italiano di Tecnologia, Naples, 80125, Italy

3Department of Chemical, Materials and Industrial Production Engineering, University of Naples Federico II, Naples, 80125, Italy

4Department of Materials Science and Engineering, Carnegie Mellon University, Pittsburgh, PA, 15213, USA

Show Author Information

Graphical Abstract

Abstract

Microelectrode arrays (MEAs) have enabled investigation of cellular networks at sub-millisecond temporal resolution. However, current MEAs are limited by the large electrode footprint since reducing the electrode’s geometric area to sub-cellular dimensions leads to a significant increase in impedance thus affecting its recording capabilities. We report a breakthrough ultra-microelectrodes platform by leveraging the outstanding surface-to-volume ratio of nanowire-templated out-of-plane synthesized three-dimensional fuzzy graphene (NT-3DFG). The enormous surface area of NT-3DFG leads to 140-fold reduction in electrode impedance compared to bare Au microelectrodes, thus enabling scaling down the geometric size by 625-fold to ca. 2 µm × 2 µm. The out-of-plane morphology of NT-3DFG leads to a tight seal with the cell membrane thus enabling recording of electrical signals with high signal-to-noise ratio (SNR) of > 6. This work highlights the possibility to push the limits of the conventional MEA technology to enable electrophysiological investigation at sub-cellular level without the need of any surface coatings. This presented approach would greatly impact our basic understanding of signal transduction within a single cell as well as complex cellular assemblies.

Keywords

microelectrode array ultra-microelectrodes electrical recordings biocompatible hybrid-nanomaterial three-dimensional (3D) graphene cardiomyocytes

Electronic Supplementary Material

Download File(s)

12274_2020_2695_MOESM1_ESM.pdf (2.1 MB)

References

[1]

Thomas,

C. A.

Jr; Springer,

P. A.

; Loeb,

G. E.

; Berwald-Netter,

; Okun,

L. M

. A miniature microelectrode array to monitor the bioelectric activity of cultured cells. Exp. Cell Res. 1972, 74, 61-66.

Crossref Google Scholar

[2]

Spira,

M. E.

; Hai,

. Multi-electrode array technologies for neuroscience and cardiology. Nat. Nanotechnol. 2013, 8, 83-94.

Crossref Google Scholar

[3]

Rastogi,

S. K.

; Kalmykov,

; Johnson,

; Cohen-Karni,

. Bioelectronics with nanocarbons. J. Mater. Chem. B 2018, 6, 7159-7178.

Crossref Google Scholar

[4]

Deku,

; Ghazavi,

; Cogan,

S. F

. Neural interfaces based on amorphous silicon carbide ultramicroelectrode arrays. Bioelectron. Med. 2018, 1, 185-200.

Crossref Google Scholar

[5]

Kozai,

T. D. Y.

; Langhals,

N. B.

; Patel,

P. R.

; Deng,

X. P.

; Zhang,

H. N.

; Smith,

K. L.

; Lahann,

; Kotov,

N. A.

; Kipke,

D. R

. Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. Nat. Mater. 2012, 11, 1065-1073.

Crossref Google Scholar

[6]

Fu,

T. M.

; Hong,

G. S.

; Zhou,

; Schuhmann,

T. G.

; Viveros,

R. D.

; Lieber,

C. M

. Stable long-term chronic brain mapping at the single-neuron level. Nat. Methods 2016, 13, 875-882.

Crossref Google Scholar

[7]

Luan,

; Wei,

X. L.

; Zhao,

Z. T.

; Siegel,

J. J.

; Potnis,

; Tuppen,

C. A.

; Lin,

S. Q.

; Kazmi,

; Fowler,

R. A.

; Holloway,

. et al. Ultraflexible nanoelectronic probes form reliable, glial scar-free neural integration. Sci. Adv. 2017, 3, e1601966.

Crossref Google Scholar

[8]

Marblestone,

A. H.

; Zamft,

B. M.

; Maguire,

Y. G.

; Shapiro,

M. G.

; Cybulski,

T. R.

; Glaser,

J. I.

; Amodei,

; Stranges,

P. B.

; Kalhor,

; Dalrymple,

D. A

. et al. Physical principles for scalable neural recording. Front. Comput. Neurosci. 2013, 7, 137.

Crossref Google Scholar

[9]

Maher,

; Pine,

; Wright,

; Tai,

Y. C

. The neurochip: A new multielectrode device for stimulating and recording from cultured neurons. J. Neurosci. Methods 1999, 87, 45-56.

Crossref Google Scholar

[10]

Gabay,

; Ben-David,

; Kalifa,

; Sorkin,

; Ze’ev,

R. A.

; Ben-Jacob,

; Hanein,

. Electro-chemical and biological properties of carbon nanotube based multi-electrode arrays. Nanotechnology 2007, 18, 035201.

Crossref Google Scholar

[11]

Meyer,

R. D.

; Cogan,

S. F.

; Nguyen,

T. H.

; Rauh,

R. D

. Electrodeposited iridium oxide for neural stimulation and recording electrodes. IEEE Trans. Neural Syst. Rehabil. Eng. 2001, 9, 2-11.

Crossref Google Scholar

[12]

Cui,

X. Y.

; Lee,

V. A.

; Raphael,

; Wiler,

J. A.

; Hetke,

J. F.

; Anderson,

D. J.

; Martin,

D. C

. Surface modification of neural recording electrodes with conducting polymer/biomolecule blends. J. Biomed. Mater. Res. 2001, 56, 261-272.

Crossref

[13]

Scanziani,

; Häusser,

. Electrophysiology in the age of light. Nature 2009, 461, 930-939.

Crossref Google Scholar

[14]

Cogan,

S. F.

; Guzelian,

A. A.

; Agnew,

W. F.

; Yuen,

T. G.

; McCreery,

D. B

. Over-pulsing degrades activated iridium oxide films used for intracortical neural stimulation. J. Neurosci. Methods 2004, 137, 141-150.

Crossref Google Scholar

[15]

Lu,

Y. C.

; Lyu,

; Richardson,

A. G.

; Lucas,

T. H.

; Kuzum,

. Flexible neural electrode array based-on porous graphene for cortical microstimulation and sensing. Sci. Rep. 2016, 6, 33526.

Crossref Google Scholar

[16]

Rastogi,

S. K.

; Bliley,

; Shiwarski,

D. J.

; Raghavan,

; Feinberg,

A. W.

; Cohen-Karni,

. Graphene microelectrode arrays for electrical and optical measurements of human stem cell-derived cardiomyocytes. Cell. Mol. Bioeng. 2018, 11, 407-418.

Crossref Google Scholar

[17]

Garg,

; Rastogi,

S. K.

; Lamparski,

; de la Barrera,

S. C.

; Pace,

G. T.

; Nuhfer,

N. T.

; Hunt,

B. M.

; Meunier,

; Cohen-Karni,

. Nanowire-mesh-templated growth of out-of-plane three-dimensional fuzzy graphene. ACS Nano 2017, 11, 6301-6311.

Crossref Google Scholar

[18]

Chen,

G. K.

; Gulbranson,

D. R.

; Hou,

Z. G.

; Bolin,

J. M.

; Ruotti,

; Probasco,

M. D.

; Smuga-Otto,

; Howden,

S. E.

; Diol,

N. R.

; Propson,

N. E

. et al. Chemically defined conditions for human iPSC derivation and culture. Nat. Methods 2011, 8, 424-429.

Crossref Google Scholar

[19]

Lian,

X. J.

; Zhang,

J. H.

; Azarin,

S. M.

; Zhu,

K. X.

; Hazeltine,

L. B.

; Bao,

X. P.

; Hsiao,

; Kamp,

T. J.

; Palecek,

S. P

. Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat. Protoc. 2013, 8, 162-175.

Crossref Google Scholar

[20]

Burridge,

P. W.

; Matsa,

; Shukla,

; Lin,

Z. C.

; Churko,

J. M.

; Ebert,

A. D.

; Lan,

; Diecke,

; Huber,

; Mordwinkin,

N. M

. et al. Chemically defined generation of human cardiomyocytes. Nat. Methods 2014, 11, 855-860.

Crossref Google Scholar

[21]

Tohyama,

; Hattori,

; Sano,

; Hishiki,

; Nagahata,

; Matsuura,

; Hashimoto,

; Suzuki,

; Yamashita,

; Satoh,

. et al. Distinct metabolic flow enables large-scale purification of mouse and human pluripotent stem cell-derived cardiomyocytes. Cell Stem Cell 2013, 12, 127-137.

Crossref Google Scholar

[22]

Rastogi,

S. K.

; Raghavan,

; Yang,

; Cohen-Karni,

. Effect of graphene on nonneuronal and neuronal cell viability and stress. Nano Lett. 2017, 17, 3297-3301.

Crossref Google Scholar

[23]

Kovács,

; Tóth,

; Hetényi,

; Málnási-Csizmadia,

; Sellers,

J. R

. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 2004, 279, 35557-35563.

Crossref Google Scholar

[24]

Li,

; Matino,

; Zhang,

; Klausen,

; McGuire,

A. F.

; Lubrano,

; Zhao,

W. T.

; Santoro,

; Cui,

B. X

. A nanostructure platform for live-cell manipulation of membrane curvature. Nat. Protoc. 2019, 14, 1772-1802.

Crossref Google Scholar

[25]

Santoro,

; Zhao,

W. T.

; Joubert,

L. M.

; Duan,

L. T.

; Schnitker,

; van de Burgt,

; Lou,

H. Y.

; Liu,

B. F.

; Salleo,

; Cui,

L. F

. et al. Revealing the cell-material interface with nanometer resolution by focused ion beam/scanning electron microscopy. ACS Nano 2017, 11, 8320-8328.

Crossref Google Scholar

[26]

Smith,

S. W

. The Scientist and Engineer's Guide to Digital Signal Processing; California Technical Pub: California, 1997.

[27]

Noda,

; Noda,

; Chen,

P. C.

; Haruta,

; Sasagawa,

; Tokuda,

; Wu,

C. Y.

; Ohta,

. Electrochemical evaluation of geometrical effect and three-dimensionalized effect of iridium oxide electrodes used for retinal stimulation. Sens. Mater. 2018, 30, 213-224.

Crossref Google Scholar

[28]

Weiland,

J. D.

; Anderson,

D. J.

; Humayun,

M. S

. In vitro electrical properties for iridium oxide versus titanium nitride stimulating electrodes. IEEE Trans. Biomed. Eng. 2002, 49, 1574-1579.

Crossref Google Scholar

[29]

Cogan,

S. F

. Neural stimulation and recording electrodes. Annu. Rev. Biomed. Eng. 2008, 10, 275-309.

Crossref Google Scholar

[30]

Rastogi,

S. K.

; Cohen-Karni,

. Nanoelectronics for neuroscience. In Encyclopedia of Biomedical Engineering; Narayan,

., Ed.; Elsevier: Amsterdam, 2019.

[31]

Kuzum,

; Takano,

; Shim,

; Reed,

J. C.

; Juul,

; Richardson,

A. G.

; de Vries,

; Bink,

; Dichter,

M. A.

; Lucas,

T. H

. et al. Transparent and flexible low noise graphene electrodes for simultaneous electrophysiology and neuroimaging. Nat. Commun. 2014, 5, 5259.

Crossref Google Scholar

[32]

Ganji,

; Kaestner,

; Hermiz,

; Rogers,

; Tanaka,

; Cleary,

; Lee,

S. H.

; Snider,

; Halgren,

; Cosgrove,

G. R

. et al. Development and translation of PEDOT: PSS microelectrodes for intraoperative monitoring. Adv. Funct. Mater. 2018, 28, 1700232.

Crossref Google Scholar

[33]

Navarrete,

E. G.

; Liang,

; Lan,

; Sanchez-Freire,

; Simmons,

; Gong,

T. Y.

; Sharma,

; Burridge,

P. W.

; Patlolla,

; Lee,

A. S

. et al. Screening drug-induced arrhythmia using human induced pluripotent stem cell-derived cardiomyocytes and low-impedance microelectrode arrays. Circulation 2013, 128, S3-S13.

Crossref Google Scholar

[34]

Yang,

; Zhou,

; Zwang,

T. J.

; Hong,

G. S.

; Zhao,

Y. L.

; Viveros,

R. D.

; Fu,

T. M.

; Gao,

; Lieber,

C. M

. Bioinspired neuron-like electronics. Nat. Mater. 2019, 18, 510-517.

Crossref Google Scholar

[35]

Xie,

; Liu,

; Fu,

T. M.

; Dai,

X. C.

; Zhou,

; Lieber,

C. M

. Three-dimensional macroporous nanoelectronic networks as minimally invasive brain probes. Nat. Mater. 2015, 14, 1286-1292.

Crossref Google Scholar

[36]

Viswam,

; Obien,

M. E. J.

; Franke,

; Frey,

; Hierlemann,

. Optimal electrode size for multi-scale extracellular-potential recording from neuronal assemblies. Front. Neurosci. 2019, 13, 385.

Crossref Google Scholar

[37]

Perry,

S. W.

; Norman,

J. P.

; Barbieri,

; Brown,

E. B.

; Gelbard,

H. A

. Mitochondrial membrane potential probes and the proton gradient: A practical usage guide. Biotechniques 2011, 50, 98-115.

Crossref Google Scholar

[38]

Kroemer,

; Galluzzi,

; Brenner,

. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 2007, 87, 99-163.

Crossref Google Scholar

[39]

Karbowski,

; Youle,

R. J

. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 2003, 10, 870-880.

Crossref Google Scholar

[40]

Hai,

; Dormann,

; Shappir,

; Yitzchaik,

; Bartic,

; Borghs,

; Langedijk,

J. P. M.

; Spira,

M. E

. Spine-shaped gold protrusions improve the adherence and electrical coupling of neurons with the surface of micro-electronic devices. J. R. Soc. Interface 2009, 6, 1153-1165.

Crossref Google Scholar

[41]

Dipalo,

; McGuire,

A. F.

; Lou,

H. Y.

; Caprettini,

; Melle,

; Bruno,

; Lubrano,

; Matino,

; Li,

; De Angelis,

. et al. Cells adhering to 3D vertical nanostructures: Cell membrane reshaping without stable internalization. Nano Lett. 2018, 18, 6100-6105.

Crossref Google Scholar

[42]

Clements,

; Thomas,

. High-throughput multi-parameter profiling of electrophysiological drug effects in human embryonic stem cell derived cardiomyocytes using multi-electrode arrays. Toxicol. Sci. 2014, 140, 445-461.

Crossref Google Scholar

[43]

Cohen-Karni,

; Casanova,

; Cahoon,

J. F.

; Qing,

; Bell,

D. C.

; Lieber,

C. M

. Synthetically encoded ultrashort-channel nanowire transistors for fast, pointlike cellular signal detection. Nano Lett. 2012, 12, 2639-2644.

Crossref Google Scholar

[44]

Cohen-Karni,

; Qing,

; Li,

; Fang,

; Lieber,

C. M

. Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Lett. 2010, 10, 1098-1102.

Crossref Google Scholar

Nano Research

Volume 13 Issue 5,
May 2020

Pages 1444-1452

DOI: 10.1007/s12274-020-2695-y

Cite this article:

Rastogi SK, Bliley J, Matino L, et al. Three-dimensional fuzzy graphene ultra-microelectrodes for sub-cellular electrical recordings. Nano Research, 2020, 13(5): 1444-1452. https://doi.org/10.1007/s12274-020-2695-y

Topics:

Electrophysiology Graphene Morphology Signal transduction

799

Views

Crossref

N/A

Web of Science

Scopus

CSCD

Google Scholar
Citation

Altmetrics

Received: 15 December 2019

Revised: 04 January 2020

Accepted: 03 February 2020

Published: 31 March 2020