Transparent and Flexible Low Noise Graphene Electrodes for Simultaneous Electrophysiology and Neuroimaging

Overview

Journal Nat Commun

Specialty Biology

Date 2014 Oct 21

PMID 25327632

Citations 136

Authors

Duygu Kuzum

Hajime Takano

Euijae Shim

Jason C Reed

Halvor Juul

Andrew G Richardson

Julius de Vries

Hank Bink

Marc A Dichter

Timothy H Lucas

Douglas A Coulter

Ertugrul Cubukcu

Brian Litt

Affiliations

Soon will be listed here.

Abstract

Calcium imaging is a versatile experimental approach capable of resolving single neurons with single-cell spatial resolution in the brain. Electrophysiological recordings provide high temporal, but limited spatial resolution, because of the geometrical inaccessibility of the brain. An approach that integrates the advantages of both techniques could provide new insights into functions of neural circuits. Here, we report a transparent, flexible neural electrode technology based on graphene, which enables simultaneous optical imaging and electrophysiological recording. We demonstrate that hippocampal slices can be imaged through transparent graphene electrodes by both confocal and two-photon microscopy without causing any light-induced artefacts in the electrical recordings. Graphene electrodes record high-frequency bursting activity and slow synaptic potentials that are hard to resolve by multicellular calcium imaging. This transparent electrode technology may pave the way for high spatio-temporal resolution electro-optic mapping of the dynamic neuronal activity.

Citing Articles

Transparent, flexible graphene-ITO-based neural microelectrodes for simultaneous electrophysiology recording and calcium imaging of intracortical neural activity in freely moving mice.

Yuan M, Li F, Xue F, Wang Y, Li B, Tang R Microsyst Nanoeng. 2025; 11(1):32.

PMID: 39994180 PMC: 11850855. DOI: 10.1038/s41378-025-00873-y.

Touch-evoked traveling waves establish a translaminar spacetime code.

Gonzales D, Khan H, Keri H, Yadav S, Steward C, Muller L Sci Adv. 2025; 11(5):eadr4038.

PMID: 39889002 PMC: 11784861. DOI: 10.1126/sciadv.adr4038.

A nanowell-based MoS neuroelectrode for high-sensitivity neural recording.

Liu S, Sun X, Wang Y, Liu K, Liu R, Zhang Y iScience. 2024; 27(10):110949.

PMID: 39391733 PMC: 11465046. DOI: 10.1016/j.isci.2024.110949.

Graphene Microelectrode Arrays, 4D Structured Illumination Microscopy, and a Machine Learning Spike Sorting Algorithm Permit the Analysis of Ultrastructural Neuronal Changes During Neuronal Signaling in a Model of Niemann-Pick Disease Type C.

Lu M, Hui E, Brockhoff M, Trauble J, Fernandez-Villegas A, Burton O Adv Sci (Weinh). 2024; 11(44):e2402967.

PMID: 39340823 PMC: 11600250. DOI: 10.1002/advs.202402967.

Transparent MXene Microelectrode Arrays for Multimodal Mapping of Neural Dynamics.

Shankar S, Chen Y, Averbeck S, Hendricks Q, Murphy B, Ferleger B Adv Healthc Mater. 2024; 14(4):e2402576.

PMID: 39328088 PMC: 11804840. DOI: 10.1002/adhm.202402576.

References

Ledochowitsch P, Olivero E, Blanche T, Maharbiz M . A transparent μECoG array for simultaneous recording and optogenetic stimulation. Annu Int Conf IEEE Eng Med Biol Soc. 2012; 2011:2937-40. DOI: 10.1109/IEMBS.2011.6090808. View

Timko B, Cohen-Karni T, Yu G, Qing Q, Tian B, Lieber C . Electrical recording from hearts with flexible nanowire device arrays. Nano Lett. 2009; 9(2):914-8. PMC: 2663853. DOI: 10.1021/nl900096z. View

Mannoor M, Tao H, Clayton J, Sengupta A, Kaplan D, Naik R . Graphene-based wireless bacteria detection on tooth enamel. Nat Commun. 2012; 3:763. DOI: 10.1038/ncomms1767. View

Wu F, Stark E, Im M, Cho I, Yoon E, Buzsaki G . An implantable neural probe with monolithically integrated dielectric waveguide and recording electrodes for optogenetics applications. J Neural Eng. 2013; 10(5):056012. PMC: 4056669. DOI: 10.1088/1741-2560/10/5/056012. View

Dombeck D, Harvey C, Tian L, Looger L, Tank D . Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat Neurosci. 2010; 13(11):1433-40. PMC: 2967725. DOI: 10.1038/nn.2648. View

Stosiek C, Garaschuk O, Holthoff K, Konnerth A . In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci U S A. 2003; 100(12):7319-24. PMC: 165873. DOI: 10.1073/pnas.1232232100. View

Benfenati V, Toffanin S, Bonetti S, Turatti G, Pistone A, Chiappalone M . A transparent organic transistor structure for bidirectional stimulation and recording of primary neurons. Nat Mater. 2013; 12(7):672-80. DOI: 10.1038/nmat3630. View

Takano H, McCartney M, Ortinski P, Yue C, Putt M, Coulter D . Deterministic and stochastic neuronal contributions to distinct synchronous CA3 network bursts. J Neurosci. 2012; 32(14):4743-54. PMC: 3328771. DOI: 10.1523/JNEUROSCI.4277-11.2012. View

Li N, Zhang X, Song Q, Su R, Zhang Q, Kong T . The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates. Biomaterials. 2011; 32(35):9374-82. DOI: 10.1016/j.biomaterials.2011.08.065. View

10.

Cogan S . Neural stimulation and recording electrodes. Annu Rev Biomed Eng. 2008; 10:275-309. DOI: 10.1146/annurev.bioeng.10.061807.160518. View

11.

Jan E, Hendricks J, Husaini V, Richardson-Burns S, Sereno A, Martin D . Layered carbon nanotube-polyelectrolyte electrodes outperform traditional neural interface materials. Nano Lett. 2009; 9(12):4012-8. DOI: 10.1021/nl902187z. View

12.

Wang X, Li X, Zhang L, Yoon Y, Weber P, Wang H . N-doping of graphene through electrothermal reactions with ammonia. Science. 2009; 324(5928):768-71. DOI: 10.1126/science.1170335. View

13.

Bae S, Kim H, Lee Y, Xu X, Park J, Zheng Y . Roll-to-roll production of 30-inch graphene films for transparent electrodes. Nat Nanotechnol. 2010; 5(8):574-8. DOI: 10.1038/nnano.2010.132. View

14.

Wang Y, Yang R, Shi Z, Zhang L, Shi D, Wang E . Super-elastic graphene ripples for flexible strain sensors. ACS Nano. 2011; 5(5):3645-50. DOI: 10.1021/nn103523t. View

15.

Reed J, Zhu H, Zhu A, Li C, Cubukcu E . Graphene-enabled silver nanoantenna sensors. Nano Lett. 2012; 12(8):4090-4. DOI: 10.1021/nl301555t. View

16.

Li N, Zhang Q, Gao S, Song Q, Huang R, Wang L . Three-dimensional graphene foam as a biocompatible and conductive scaffold for neural stem cells. Sci Rep. 2013; 3:1604. PMC: 3615386. DOI: 10.1038/srep01604. View

17.

Balandin A, Ghosh S, Bao W, Calizo I, Teweldebrhan D, Miao F . Superior thermal conductivity of single-layer graphene. Nano Lett. 2008; 8(3):902-7. DOI: 10.1021/nl0731872. View

18.

Schedin F, Geim A, Morozov S, Hill E, Blake P, Katsnelson M . Detection of individual gas molecules adsorbed on graphene. Nat Mater. 2007; 6(9):652-5. DOI: 10.1038/nmat1967. View

19.

Cardin J, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K . Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat Protoc. 2010; 5(2):247-54. PMC: 3655719. DOI: 10.1038/nprot.2009.228. View

20.

Lempka S, Johnson M, Barnett D, Moffitt M, Otto K, Kipke D . Optimization of microelectrode design for cortical recording based on thermal noise considerations. Conf Proc IEEE Eng Med Biol Soc. 2007; 2006:3361-4. DOI: 10.1109/IEMBS.2006.259432. View