Nongenetic optical control of neurons is a powerful technique to study and manipulate the function of the nervous system. This research has benchmarked the performance of organic electrolytic photocapacitor (OEPC) optoelectronic stimulators at the level of single mammalian cells: human embryonic kidney (HEK) cells with heterologously expressed voltage-gated K+ channels and hippocampal primary neurons. OEPCs act as extracellular stimulation electrodes driven by deep red light. The electrophysiological recordings show that millisecond light stimulation of OEPC shifts conductance-voltage plots of voltage-gated K+ channels by ≈30 mV. Models are described both for understanding the experimental findings at the level of K+ channel kinetics in HEK cells, as well as elucidating interpretation of membrane electrophysiology obtained during stimulation with an electrically floating extracellular photoelectrode. A time-dependent increase in voltage-gated channel conductivity in response to OEPC stimulation is demonstrated. These findings are then carried on to cultured primary hippocampal neurons. It is found that millisecond time-scale optical stimuli trigger repetitive action potentials in these neurons. The findings demonstrate that OEPC devices enable the manipulation of neuronal signaling activities with millisecond precision. OEPCs can therefore be integrated into novel in vitro electrophysiology protocols, and the findings can inspire in vivo applications.

Bioelectronics Materials and Devices Laboratory Central European Institute of Technology Brno University of Technology Purkyňova 123 Brno 61200 Czech Republic

BioTechMed Graz Graz 8010 Austria

Department of Pharmacology Toxicology and Clinical Pharmacy Institute of Pharmacy University of Tuebingen Auf der Morgenstelle 8 72076 Tuebingen Germany

Department of Physics Faculty of Science University of Zagreb Bijenička c 32 Zagreb 10000 Croatia

Gottfried Schatz Research Center Chair of Biophysics Medical University of Graz Neue Stiftingtalstraße 6 Graz 8010 Austria

Gottfried Schatz Research Center Division of Cell Biology Histology and Embryology Medical University of Graz Neue Stiftingtalstraße 6 Graz 8010 Austria

Gottfried Schatz Research Center Molecular Biology and Biochemistry Medical University of Graz Neue Stiftingtalstraße 6 6 Graz 8010 Austria

Institute of Health Care Engineering with European Testing Center of Medical Devices Graz University of Technology Graz 8010 Austria

NMI Natural and Medical Sciences Institute at the University of Tuebingen 72770 Reutlingen Germany

Research Unit of Experimental Neurotraumatology Department of Neurosurgery Medical University Graz Auenbruggerplatz 2 2 Graz 8036 Austria

Zobrazit více v PubMed

Beitz J. M., Front. Biosci. 2014, 6, 65. PubMed

Velasco F., Jiménez F., Pérez M. L., Carrillo‐Ruiz J. D., Velasco A. L., Ceballos J., Velasco M., Neurosurgery 2001, 49, 293; discussion 306–8. PubMed

Shapiro S., World Neurosurg. 2014, 81, 830. PubMed

Borgens R. B., Roederer E., Cohen M. J., Science 1981, 213, 611. PubMed

Humayun M. S., Dorn J. D., Da Cruz L., Dagnelie G., Sahel J.‐ A., Stanga P. E., Cideciyan A. V., Duncan J. L., Eliott D., Filley E., Ho A. C., Santos A., Safran A. B., Arditi A., Del Priore L. V., Greenberg R. J., Ophthalmology 2012, 119, 779. PubMed PMC

Zrenner E., Bartz‐Schmidt K. U., Benav H., Besch D., Bruckmann A., Gabel V.‐P., Gekeler F., Greppmaier U., Harscher A., Kibbel S., Koch J., Kusnyerik A., Peters T., Stingl K., Sachs H., Stett A., Szurman P., Wilhelm B., Wilke R., Proc. Biol. Sci. 2011, 278, 1489. PubMed PMC

Ghezzi D., Front. Neurosci. 2015, 9, 290. PubMed PMC

Klinke R., Kral A., Heid S., Tillein J., Hartmann R., Science 1999, 285, 1729. PubMed

Kral A., Sharma A., Trends Neurosci. 2012, 35, 111. PubMed PMC

Asplund M., Nyberg T., Inganäs O., Polym. Chem. 2010, 1, 1374.

Jacques S. L., Phys. Med. Biol. 2013, 58, R37. PubMed

Mathieson K., Loudin J., Goetz G., Huie P., Wang L., Kamins T. I., Galambos L., Smith R., Harris J. S., Sher A., Palanker D., Nat. Photonics 2012, 6, 391. PubMed PMC

Someya T., Bao Z., Malliaras G. G., Nature 2016, 540, 379. PubMed

Rand D., Jakešová M., Lubin G., Vėbraitė I., David‐Pur M., Đerek V., Cramer T., Sariciftci N. S., Hanein Y., Głowacki E. D., Adv. Mater. 2018, 30, 1707292. PubMed

Jakešová M., Ejneby M. S., Đerek V., Schmidt T., Gryszel M., Brask J., Schindl R., Simon D. T., Berggren M., Elinder F., Głowacki E. D., Sci. Adv. 2019, 5, eaav5265. PubMed PMC

Silverå Ejneby M., Migliaccio L., Gicevičius M., Đerek V., Jakešová M., Elinder F., Głowacki E. D., Adv. Mater. Technol. 2020, 5, 1900860.

Ðerek V., Rand D., Migliaccio L., Hanein Y., Głowacki E. D., Front. Bioeng. Biotechnol. 2020, 8, 284. PubMed PMC

Silverå Ejneby M., Jakešová M., Ferrero J. J., Migliaccio L., Sahalianov I., Zhao Z., Berggren M., Khodagholy D., Đerek V., Gelinas J. N., Głowacki E. D., Nat. Biomed. Eng. 2021, 10.1038/s41551-021-00817-7. PubMed DOI

Bezanilla F., Physiol. Rev. 2000, 80, 555. PubMed

Bezanilla F., Nat. Rev. Mol. Cell Biol. 2008, 9, 323. PubMed

Schoen I., Fromherz P., Biophys. J. 2007, 92, 1096. PubMed PMC

Bezanilla F., J. Gen. Physiol. 2018, 150, 911. PubMed PMC

Bischof H., Burgstaller S., Springer A., Matt L., Rauter T., Bachkönig O. A., Schmidt T., Groschner K., Schindl R., Madl T., Plesnila N., Lukowski R., Graier W. F., Malli R., iScience 2021, 24, 102346. PubMed PMC

Tiapko O., Shrestha N., Lindinger S., Guedes De La Cruz G., Graziani A., Klec C., Butorac C., Graier W. F., Kubista H., Freichel M., Birnbaumer L., Romanin C., Glasnov T., Groschner K., Chem. Sci. 2019, 10, 2837. PubMed PMC

Hoťka M., Zahradník I., PLoS One 2017, 12, e0188452. PubMed PMC

Hou P., Zhang R., Liu Y., Feng J., Wang W., Wu Y., Ding J., PLoS One 2014, 9, e89975. PubMed PMC

Destexhe A., Huguenard J. R., Computational Modeling Methods for Neuroscientists, The MIT Press, Cambridge, MA: 2009.

Langthaler S., Šajić J. L., Rienmüller T., Weinberg S. H., Baumgartner C., Cells 2022, 11, 239. PubMed PMC

Stoppacher S., Scheruebel S., Üçal M., Kornmüller K., Głowacki E., Schindl R., Shrestha N., Schmidt T., Baumgartner C., Rienmüller T., Stud. Health Technol. Inf. 2020, 271, 9. PubMed

Langthaler S., Rienmüller T., Scheruebel S., Pelzmann B., Shrestha N., Zorn‐Pauly K., Schreibmayer W., Koff A., Baumgartner C., PLoS Comput. Biol. 2021, 17, e1009091. PubMed PMC

Głowacki E. D., Voss G., Sariciftci N. S., Adv. Mater. 2013, 25, 6783. PubMed

Merrill D. R., Bikson M., Jefferys J. G. R., J. Neurosci. Methods 2005, 141, 171. PubMed

Schoen I., Fromherz P., J. Neurophysiol. 2008, 100, 346. PubMed

Srivastava S. B., Melikov R., Yildiz E., Dikbas U. M., Sadeghi S., Kavakli I. H., Sahin A., Nizamoglu S., J. Mater. Chem. C 2021, 9, 1755.

Srivastava S. B., Melikov R., Yildiz E., Han M., Sahin A., Nizamoglu S., Biomed. Opt. Express 2020, 11, 5237. PubMed PMC

Gautam V., Rand D., Hanein Y., Narayan K. S., Adv. Mater. 2014, 26, 1751. PubMed

Ghezzi D., Antognazza M. R., Dal Maschio M., Lanzarini E., Benfenati F., Lanzani G., Nat. Commun. 2011, 2, 166. PubMed

Ghezzi D., Antognazza M. R., Maccarone R., Bellani S., Lanzarini E., Martino N., Mete M., Pertile G., Bisti S., Lanzani G., Benfenati F., Nat. Photonics 2013, 7, 400. PubMed PMC

Palanker D., Głowacki E. D., Ghezzi D., Nat. Nanotechnol. 2021, 16, 1330. PubMed PMC

Jiang Y., Parameswaran R., Li X., Carvalho‐De‐Souza J. L., Gao X., Meng L., Bezanilla F., Shepherd G. M. G., Tian B., Nat. Protoc. 2019, 14, 1339. PubMed PMC

Carvalho‐De‐Souza J. L., Treger J. S., Dang B., Kent S. B. H., Pepperberg D. R., Bezanilla F., Neuron 2015, 86, 207. PubMed PMC

Shapiro M. G., Homma K., Villarreal S., Richter C. ‐P., Bezanilla F., Nat. Commun. 2012, 3, 736. PubMed PMC

Jiang Y., Carvalho‐De‐Souza J. L., Wong R. C. S., Luo Z., Isheim D., Zuo X., Nicholls A. W., Jung I. W., Yue J., Liu D.‐J., Wang Y., De Andrade V., Xiao X., Navrazhnykh L., Weiss D. E., Wu X., Seidman D. N., Bezanilla F., Tian B., Nat. Mater. 2016, 15, 1023. PubMed PMC

Light-Controlled Electric Stimulation with Organic Electrolytic Photocapacitors Achieves Complex Neuronal Network Activation: Semi-Chronic Study in Cortical Cell Culture and Rat Model

Photo-Chemical Stimulation of Neurons with Organic Semiconductors