Recent advances in light-responsive materials enabled the development of devices that can wirelessly activate tissue with light. Here it is shown that solution-processed organic heterojunctions can stimulate the activity of primary neurons at low intensities of light via photochemical reactions. The p-type semiconducting polymer PDCBT and the n-type semiconducting small molecule ITIC (a non-fullerene acceptor) are coated on glass supports, forming a p-n junction with high photosensitivity. Patch clamp measurements show that low-intensity white light is converted into a cue that triggers action potentials in primary cortical neurons. The study shows that neat organic semiconducting p-n bilayers can exchange photogenerated charges with oxygen and other chemical compounds in cell culture conditions. Through several controlled experimental conditions, photo-capacitive, photo-thermal, and direct hydrogen peroxide effects on neural function are excluded, with photochemical delivery being the possible mechanism. The profound advantages of low-intensity photo-chemical intervention with neuron electrophysiology pave the way for developing wireless light-based therapy based on emerging organic semiconductors.

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

Biological and Environmental Science and Engineering King Abdullah University of Science and Technology Thuwal 23955 6900 Saudi Arabia

Department of Chemical Engineering and Biotechnology University of Cambridge Cambridge CB30AS UK

Department of Chemistry and Centre for Processable Electronics Imperial College London London W12 0BZ UK

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

Physical Science and Engineering Thuwal 23955 6900 Saudi Arabia

Zobrazit více v PubMed

Hamblin M. R., Nelson S. T., Strahan J. R., Photobiomodulation, Photomed., Laser Surg. 2018, 36, 241. PubMed PMC

Chan W.‐M., Lam D. S. C., Lai T. Y. Y., Liu D. T. L., Li K. K. W., Yao Y., Wong T.‐H., Ophthalmology 2004, 111, 1576. PubMed

Maya‐Vetencourt J. F., Ghezzi D., Antognazza M. R., Colombo E., Mete M., Feyen P., Desii A., Buschiazzo A., Di Paolo M., Di Marco S., Ticconi F., Emionite L., Shmal D., Marini C., Donelli I., Freddi G., Maccarone R., Bisti S., Sambuceti G., Pertile G., Lanzani G., Benfenati F., Nat. Mater. 2017, 16, 681. PubMed PMC

Berggren M., Głowacki E. D., Simon D. T., Stavrinidou E., Tybrandt K., Chem. Rev. 2022, 122, 4826. PubMed PMC

Rohringer S., Holnthoner W., Chaudary S., Slezak P., Priglinger E., Strassl M., Pill K., Mühleder S., Redl H., Dungel P., Sci. Rep. 2017, 7, 10700. PubMed PMC

Chen R., Gore F., Nguyen Q.‐A., Ramakrishnan C., Patel S., Kim S. H., Raffiee M., Kim Y. S., Hsueh B., Krook‐Magnusson E., Soltesz I., Deisseroth K., Nat. Biotechnol. 2021, 39, 161. PubMed PMC

Maiti D., Tong X., Mou X., Yang K., Front Pharmacol 2019, 9, 1401. PubMed PMC

Vines J. B., Yoon J.‐H., Ryu N.‐E., Lim D.‐J., Park H., Front Chem 2019, 7, 167. PubMed PMC

Parameswaran R., Carvalho‐de‐Souza J. L., Jiang Y., Burke M. J., Zimmerman J. F., Koehler K., Phillips A. W., Yi J., Adams E. J., Bezanilla F., Tian B., Nat. Nanotechnol. 2018, 13, 260. PubMed PMC

Jiang Y., Li X., Liu B., Yi J., Fang Y., Shi F., Gao X., Sudzilovsky E., Parameswaran R., Koehler K., Nair V., Yue J., Guo K., Fang Y., Tsai H.‐M., Freyermuth G., Wong R. C. S., Kao C.‐M., Chen C.‐T., Nicholls A. W., Wu X., Shepherd G. M. G., Tian B., Nat. Biomed. Eng. 2018, 2, 508. PubMed PMC

Silverå‐Ejneby M., Jakešová M., Ferrero J. J., Migliaccio L., Zhao Z., Berggren M., Khodagholy D., Đerek V., Gelinas J., Głowacki E. D., bioRxiv 2020, 2020.07.01.182113.

Martino N., Feyen P., Porro M., Bossio C., Zucchetti E., Ghezzi D., Benfenati F., Lanzani G., Antognazza M. R., Sci. Rep. 2015, 5, 8911. PubMed PMC

Tortiglione C., Antognazza M. R., Tino A., Bossio C., Marchesano V., Bauduin A., Zangoli M., Morata S. V., Lanzani G., Sci. Adv. 2017, 3, e1601699. PubMed PMC

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

Benfenati V., Martino N., Antognazza M. R., Pistone A., Toffanin S., Ferroni S., Lanzani G., Muccini M., Adv. Healthcare Mater. 2014, 3, 306. PubMed

Lodola F., Rosti V., Tullii G., Desii A., Tapella L., Catarsi P., Lim D., Moccia F., Antognazza M. R., Sci. Adv. 2019, 5, eaav4620. PubMed PMC

Zangoli M., Di Maria F., Zucchetti E., Bossio C., Antognazza M. R., Lanzani G., Mazzaro R., Corticelli F., Baroncini M., Barbarella G., Nanoscale 2017, 9, 9202. PubMed

Abdel Aziz I., Malferrari M., Roggiani F., Tullii G., Rapino S., Antognazza M. R., iScience 2020, 23, 101091. PubMed PMC

Antognazza M. R., Abdel Aziz I., Lodola F., Oxid Med Cell Longevity 2019, 2019, 2867516. PubMed PMC

Moros M., Lewinska A., Onorato G., Antognazza M. R., Di Francesca M., Blasio M., Lanzani G., Tino A., Wnuk M., Tortiglione C., MRS Commun. 2018, 8, 918.

Hopkins J., Travaglini L., Lauto A., Cramer T., Fraboni B., Seidel J., Mawad D., Adv. Mater. Technol. 2019, 4, 1800744.

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

Knupfer M., Appl. Phys. A 2003, 77, 623.

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

Paltrinieri T., Bondi L., Đerek V., Fraboni B., Głowacki E. D., Cramer T., Adv. Funct. Mater. 2021, 31, 2010116.

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

Vaquero S., Bossio C., Bellani S., Martino N., Zucchetti E., Lanzani G., Antognazza M. R., J. Mater. Chem. B 2016, 4, 5272. 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.

Schmidt T., Jakešová M., Đerek V., Kornmueller K., Tiapko O., Bischof H., Burgstaller S., Waldherr L., Nowakowska M., Baumgartner C., Üçal M., Leitinger G., Scheruebel S., Patz S., Malli R., Głowacki E. D., Rienmüller T., Schindl R., Adv. Mater. Technol. 2022, 7, 2101159. PubMed PMC

Jakešová M., Silverå Ejneby M., 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

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

Wadsworth A., Moser M., Marks A., Little M. S., Gasparini N., Brabec C. J., Baran D., McCulloch I., Chem. Soc. Rev. 2019, 48, 1596. PubMed

Benov L., Med Princ Pract 2015, 24, 14. PubMed PMC

Savva A., Wustoni S., Inal S., J. Mater. Chem. C 2018, 6, 12023.

Jakešová M., Apaydin D. H., Sytnyk M., Oppelt K., Heiss W., Sariciftci N. S., Głowacki E. D., Adv. Funct. Mater. 2016, 26, 5248.

Migliaccio L., Gryszel M., Đerek V., Pezzella A., Głowacki E. D., Mater. Horiz. 2018, 5, 984.

Suppes G. M., Fortin P. J., Holdcroft S., J. Electrochem. Soc. 2015, 162, H551.

Gryszel M., Sytnyk M., Jakešová M., Romanazzi G., Gabrielsson R., Heiss W., Głowacki E. D., ACS Appl. Mater. Interfaces 2018, 10, 13253. PubMed

Ribeiro L. A., Oliveira Neto P. H., da Cunha W. F., Roncaratti L. F., Gargano R., da Silva Filho D. A., e Silva G. M., J. Chem. Phys. 2011, 135, 224901. PubMed

Neher E., Sakmann B., Nature 1976, 260, 799. PubMed

Häusser M., Raman I. M., Otis T., Smith S. L., Nelson A., du Lac S., Loewenstein Y., Mahon S., Pennartz C., Cohen I., Yarom Y., J. Neurosci. 2004, 24, 9215. PubMed PMC

Dégenètais E., Thierry A.‐M., Glowinski J., Gioanni Y., Cereb Cortex 2002, 12, 1. PubMed

Lodola F., Martino N., Tullii G., Lanzani G., Antognazza M. R., Sci. Rep. 2017, 7, 8477. PubMed PMC

Zhao G., Chasteen N. D., Anal. Biochem. 2006, 349, 262. PubMed

Grady J. K., Chasteen N. D., Harris D. C., Anal. Biochem. 1988, 173, 111. PubMed

Kirsch M., Lomonosova E. E., Korth H.‐G., Sustmann R., de Groot H., J. Biol. Chem. 1998, 273, 12716. PubMed

Carette B., J Neurophysiol 1998, 80, 1042. PubMed

Yamada‐Hanff J., Bean B. P., J. Neurosci. 2013, 33, 15011. PubMed PMC

Deitmer J. W., Szatkowski M., J Physiol 1990, 421, 617. PubMed PMC

Holliday S., Ashraf R. S., Wadsworth A., Baran D., Yousaf S. A., Nielsen C. B., Tan C.‐H., Dimitrov S. D., Shang Z., Gasparini N., Alamoudi M., Laquai F., Brabec C. J., Salleo A., Durrant J. R., McCulloch I., Nat. Commun. 2016, 7, 11585. PubMed PMC

Gryszel M., Markov A., Vagin M., Głowacki E. D., J. Mater. Chem. A 2018, 6, 24709.

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