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Micelle-enabled self-assembly of porous and monolithic carbon membranes for bioelectronic interfaces

Abstract

Real-world bioelectronics applications, including drug delivery systems, biosensing and electrical modulation of tissues and organs, largely require biointerfaces at the macroscopic level. However, traditional macroscale bioelectronic electrodes usually exhibit invasive or power-inefficient architectures, inability to form uniform and subcellular interfaces, or faradaic reactions at electrode surfaces. Here, we develop a micelle-enabled self-assembly approach for a binder-free and carbon-based monolithic device, aimed at large-scale bioelectronic interfaces. The device incorporates a multi-scale porous material architecture, an interdigitated microelectrode layout and a supercapacitor-like performance. In cell training processes, we use the device to modulate the contraction rate of primary cardiomyocytes at the subcellular level to target frequency in vitro. We also achieve capacitive control of the electrophysiology in isolated hearts, retinal tissues and sciatic nerves, as well as bioelectronic cardiac sensing. Our results support the exploration of device platforms already used in energy research to identify new opportunities in bioelectronics.

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Fig. 1: Hierarchical porous carbon synthesis and characterization.
Fig. 2: Device fabrication and characterization.
Fig. 3: In vitro biological training.
Fig. 4: Biological modulation at the tissue and organ level.

Data availability

The raw data that support the findings of this study are available from the corresponding authors upon reasonable request. The LabVIEW control program, and the MATLAB and Python scripts are available at https://github.com/uchicago-Tian-Lab/Fang_et_al_Nat_Nanotechnology_2020.

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Acknowledgements

This work is supported by the National Institutes of Health (NIH NS101488), Army Research Office (W911NF-18-1-0042), National Science Foundation (NSF CMMI-1848613) and Office of Naval Research (PECASE, N000141612958).

Author information

Affiliations

Authors

Contributions

Y.F. and B.T. conceived the concept of this manuscript. Y.F., A.P. and L.M. fabricated the carbon micro-supercapacitor-like devices. Y.L., A.P. and Y.F. conducted the electrochemistry characterizations. A.P. and L.M. conducted the COMSOL simulations. Y.F. and A.P. performed the in vitro cardiac pacing experiments. M.Y.R., A.P. and L.M. conducted the isolated heart experiments. H.A.L. and W.W. conducted the retina stimulation experiments. A.P., L.M., J.Y., M.Y.R. and B.E. conducted the nerve stimulation experiments. J.Y. and Y.F. conducted the in vitro and in vivo biocompatibility experiments. E.S. and N.Y. assisted in the in vitro culture and imaging. J.J., E.S. and Y.J. helped with data analysis. All authors contributed to the preparation of the manuscript.

Corresponding authors

Correspondence to Yin Fang or Bozhi Tian.

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The authors declare no competing interests.

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Peer review information Nature Nanotechnology thanks the anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–29, Tables 1–2 and Notes 1–3.

Reporting Summary

Supplementary Video 1

The ΔF/F0 video of CMs at the beginning of the subthreshold training. Overlay shows approximate positions of the cells. Scale bar, 10 μm.

Supplementary Video 2

The ΔF/F0 video of CMs at the end of the subthreshold training. Overlay shows approximate positions of the cells and was adjusted for the field of view drift with respect to Supplementary Video 1. Scale bar, 10 μm.

Supplementary Video 3

Representative video of the isolated heart stimulated to a frequency of 3.33 Hz.

Supplementary Video 4

Representative video of the sciatic nerve stimulated on one limb.

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Fang, Y., Prominski, A., Rotenberg, M.Y. et al. Micelle-enabled self-assembly of porous and monolithic carbon membranes for bioelectronic interfaces. Nat. Nanotechnol. 16, 206–213 (2021). https://doi.org/10.1038/s41565-020-00805-z

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