Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

A polymer optoelectronic interface restores light sensitivity in blind rat retinas

Nature Photonics volume 7, pages 400–406 (2013)Cite this article

Subjects

Abstract

Interfacing organic electronics with biological substrates offers new possibilities for biotechnology by taking advantage of the beneficial properties exhibited by organic conducting polymers. These polymers have been used for cellular interfaces in several applications, including cellular scaffolds, neural probes, biosensors and actuators for drug release. Recently, an organic photovoltaic blend has been used for neuronal stimulation via a photo-excitation process. Here, we document the use of a single-component organic film of poly(3-hexylthiophene) (P3HT) to trigger neuronal firing upon illumination. Moreover, we demonstrate that this bio–organic interface restores light sensitivity in explants of rat retinas with light-induced photoreceptor degeneration. These findings suggest that all-organic devices may play an important future role in subretinal prosthetic implants.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Characterization of the photostimulus generated by the polymeric interface.
Figure 2: Photovoltaic excitation of neurons mediated by a P3HT active layer.
Figure 3: The photoreceptor layer is replaced in the degenerate retina by the organic polymer.
Figure 4: The P3HT layer restores responses in blind retinas.

Similar content being viewed by others

References

  1. Ethier, C., Oby, E. R., Bauman, M. J. & Miller, L. E. Restoration of grasp following paralysis through brain-controlled stimulation of muscles. Nature 485, 368–371 (2012).

    Article  ADS  Google Scholar 

  2. Moritz, C. T., Perlmutter, S. I. & Fetz, E. E. Direct control of paralysed muscles by cortical neurons. Nature 456, 639–642 (2008).

    Article  ADS  Google Scholar 

  3. Fasano, A., Daniele, A. & Albanese, A. Treatment of motor and non-motor features of Parkinson's disease with deep brain stimulation. Lancet Neurol. 11, 429–442 (2012).

    Article  Google Scholar 

  4. Shannon, R. V. Advances in auditory prostheses. Curr. Opin. Neurol. 25, 61–66 (2012).

    Article  Google Scholar 

  5. Mathieson, K. et al. Photovoltaic retinal prosthesis with high pixel density. Nature Photon. 6, 391–397 (2012).

    Article  ADS  Google Scholar 

  6. Zrenner, E. et al. Subretinal electronic chips allow blind patients to read letters and combine them to words. Proc. R. Soc. B 278, 1489–1497 (2011).

    Article  Google Scholar 

  7. Ahuja, A. K. et al. Blind subjects implanted with the Argus II retinal prosthesis are able to improve performance in a spatial-motor task. Br. J. Ophthalmol. 95, 539–543 (2011).

    Article  Google Scholar 

  8. Pastrana, E. Optogenetics: controlling cell function with light. Nature Methods 8, 24–49 (2010).

    Article  Google Scholar 

  9. Mattis, J. et al. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nature Methods 9, 159–231 (2012).

    Article  Google Scholar 

  10. Wallace, G. G., Moulton, S. E. & Clark, G. M. Electrode–cellular interface. Science 324, 185–186 (2009).

    Article  ADS  Google Scholar 

  11. Owens, R. M. & Malliaras, G. G. Organic electronics at the interface with biology. MRS Bull. 35, 449–456 (2010).

    Article  Google Scholar 

  12. Moulton, S. E., Higgins, M. J., Kapsa, R. M. I. & Wallace, G. G. Organic bionics: a new dimension in neural communications. Adv. Funct. Mater. 22, 2003–2014 (2012).

    Article  Google Scholar 

  13. Bystrenova, E. et al. Neural networks grown on organic semiconductors. Adv. Funct. Mater. 18, 1751–1756 (2008).

    Article  Google Scholar 

  14. Bolin, M. H. et al. Nano-fiber scaffold electrodes based on PEDOT for cell stimulation. Sens. Actuat. B 142, 451–456 (2009).

    Article  Google Scholar 

  15. Abidian, M. R., Ludwig, K. A., Marzullo, T. C., Martin, D. C. & Kipke, D. R. Interfacing conducting polymer nanotubes with the central nervous system: chronic neural recording using poly (3,4-ethylenedioxythiophene) nanotubes. Adv. Mater. 21, 3764–3770 (2009).

    Article  Google Scholar 

  16. Richardson-Burns, S. M. et al. Polymerization of the conducting polymer poly(3,4-ethylenedioxythiophene) (PEDOT) around living neural cells. Biomaterials 28, 1539–1552 (2007).

    Article  Google Scholar 

  17. Gerard, M., Chaubey, A. & Malhotra, B. D. Application of conducting polymers to biosensors. Biosens. Bioelectr. 17, 345–359 (2002).

    Article  Google Scholar 

  18. Arshak, K., Velusamy, V., Korostynska, O., Oliwa-Stasiak, K. & Adley, C. Conducting polymers and their applications to biosensors: emphasizing on foodborne pathogen detection. IEEE Sens. J 9, 1942–1951 (2009).

    Article  ADS  Google Scholar 

  19. Simon, D. T. et al. Organic electronics for precise delivery of neurotransmitters to modulate mammalian sensory function. Nature Mater. 8, 742–746 (2009).

    Article  ADS  Google Scholar 

  20. Richardson, R. T. et al. Polypyrrole-coated electrodes for the delivery of charge and neurotrophins to cochlear neurons. Biomaterials 30, 2614–2624 (2009).

    Article  Google Scholar 

  21. Wan, A. M. D., Brooks, D. J., Gumus, A., Fischbach, C. & Malliaras, G. G. Electrical control of cell density gradients on a conducting polymer surface. Chem. Commun. 5278–5280 (2009).

  22. Schmidt, C. E., Shastri, V. R., Vacanti, J. P. & Langer, R. Stimulation of neurite outgrowth using an electrically conducting polymer. Proc. Natl Acad. Sci. USA 94, 8948–8953 (1997).

    Article  ADS  Google Scholar 

  23. Svennersten, K., Bolin, M. H., Jager, E. W. H., Berggren, M. & Richter-Dahlfors, A. Electrochemical modulation of epithelia formation using conducting polymers. Biomaterials 30, 6257–6264 (2009).

    Article  Google Scholar 

  24. Blau, A. et al. Flexible, all-polymer microelectrode arrays for the capture of cardiac and neuronal signals. Biomaterials 32, 1778–1786 (2011).

    Article  Google Scholar 

  25. Antognazza, M. R., Ghezzi, D., Musitelli, D., Garbugli, M. & Lanzani, G. A hybrid solid–liquid polymer photodiode for the bioenvironment. Appl. Phys. Lett. 94, 243501 (2009).

    Article  ADS  Google Scholar 

  26. Ghezzi, D. et al. A hybrid bioorganic interface for neuronal photoactivation. Nature Commun. 2, 166 (2011).

    Article  ADS  Google Scholar 

  27. Pappas, T. C. et al. Nanoscale engineering of a cellular interface with semiconductor nanoparticle films for photoelectric stimulation of neurons. Nano Lett. 7, 513–519 (2007).

    Article  ADS  Google Scholar 

  28. Goda, Y. & Colicos, M. A. Photoconductive stimulation of neurons cultured on silicon wafers. Nature Protoc. 1, 461–467 (2006).

    Article  Google Scholar 

  29. Kong, L. & Zepp, R. G. Production and consumption of reactive oxygen species by fullerenes. Environ. Toxicol. Chem. 31, 136–143 (2012).

    Article  Google Scholar 

  30. Jacobson, S. G. & Cideciyan, A. V. Treatment possibilities for retinitis pigmentosa. N. Engl. J. Med. 363, 1669–1671 (2010).

    Article  Google Scholar 

  31. MacLaren, R. E. et al. Retinal repair by transplantation of photoreceptor precursors. Nature 444, 203–207 (2006).

    Article  ADS  Google Scholar 

  32. Pearson, R. A. et al. Restoration of vision after transplantation of photoreceptors. Nature 485, 99–103 (2012).

    Article  ADS  Google Scholar 

  33. Koch, S. et al. Gene therapy restores vision and delays degeneration in the CNGB1–/– mouse model of retinitis pigmentosa. Hum. Mol. Genet. 21, 4486–4496 (2012).

    Article  Google Scholar 

  34. Busskamp, V. et al. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329, 413–417 (2010).

    Article  ADS  Google Scholar 

  35. Bi, A. D. et al. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50, 23–33 (2006).

    Article  Google Scholar 

  36. Zrenner, E. Artificial vision: solar cells for the blind. Nature Photon. 6, 342–343 (2012).

    Article  ADS  Google Scholar 

  37. Polosukhina, A. et al. Photochemical restoration of visual responses in blind mice. Neuron 75, 271–353 (2012).

    Article  Google Scholar 

  38. Natoli, R. et al. Gene and noncoding RNA regulation underlying photoreceptor protection: microarray study of dietary antioxidant saffron and photobiomodulation in rat retina. Mol. Vision 16, 1801–1823 (2010).

    Google Scholar 

  39. Valter, K. et al. Time course of neurotrophic factor upregulation and retinal protection against light-induced damage after optic nerve section. Invest. Ophthalmol. Vis. Sci. 46, 1748–1754 (2005).

    Article  Google Scholar 

  40. Delori, F. C., Webb, R. H. & Sliney, D. H. Maximum permissible exposures for ocular safety (ANSI 2000), with emphasis on ophthalmic devices. J. Opt. Soc. Am. A 24, 1250–1265 (2007).

    Article  ADS  Google Scholar 

  41. Sliney, D. Exposure geometry and spectral environment determine photobiological effects on the human eye. Photochem. Photobiol. 81, 483–489 (2005).

    Article  Google Scholar 

  42. Butterwick, A. et al. in Proc. SPIE 6426, Ophthalmic Technologies XVII, paper 64260R (eds Stuck, B. E. et al.) (SPIE, 2007).

Download references

Acknowledgements

The authors thank M. Nanni, G. Pruzzo and F. Succol for technical advice and M. dal Maschio and P. Baldelli for help with data interpretation and discussions. The authors also thank A.J. Heeger, P. Greengard, L.M. Chalupa and L. Maffei for critical reading of the manuscript. The research was supported by the FP7-PEOPLE-212-ITN (‘OLIMPIA’ grant #316832), the Fondazione Istituto Italiano di Tecnologia (‘Multidisciplinary Projects’) and Telethon – Italy (GGP12033 grant to G.L., F.B. and S.B.). The authors also acknowledge support from M. Monti and by R. and I. Munari Gloder. The manuscript was revised by the American Journal Experts editing organization.

Author information

Authors and Affiliations

  1. Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Genova 16163, Italy

    Diego Ghezzi & Fabio Benfenati

  2. Center for Nano Science and Technology@PoliMi, Istituto Italiano di Tecnologia, Milano 20133, Italy

    Maria Rosa Antognazza, Sebastiano Bellani, Erica Lanzarini, Nicola Martino & Guglielmo Lanzani

  3. Dipartimento di Tecnologie Biomediche, Università dell'Aquila, L'Aquila, 67100, Italy

    Rita Maccarone & Silvia Bisti

  4. Department of Physics, Politecnico di Milano, Piazza L. Da Vinci 32, Milano, 20133, Italy

    Sebastiano Bellani, Nicola Martino & Guglielmo Lanzani

  5. UO Oculistica, Ospedale S. Cuore-Don Calabria, Negrar 37024, Italy

    Maurizio Mete & Grazia Pertile

  6. Department of Experimental Medicine, University of Genova, Genova, 16163, Italy

    Fabio Benfenati

Authors
  1. Diego Ghezzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Rosa Antognazza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rita Maccarone
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sebastiano Bellani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Erica Lanzarini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicola Martino
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maurizio Mete
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Grazia Pertile
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Silvia Bisti
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Guglielmo Lanzani
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Fabio Benfenati
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.G. prepared cell cultures, degenerate animals and retinal explants, planned experiments, performed photostimulation experiments and cell viability assays, analysed data and wrote the manuscript. M.R.A. planned the experiments, discussed the results and wrote the manuscript. R.M. prepared degenerate animals, performed retinal sections and acquired confocal images. E.L. prepared polymer samples. S.Be., E.L. and N.M. performed polymer-film electro-optical characterization and analysed data. M.M. and G.P. discussed results. S.Bi. discussed electrophysiological experiments with retinal explants. G.L. and F.B. planned experiments, interpreted and discussed the data, wrote the manuscript and supported the research. All authors discussed the results and revised the manuscript.

Corresponding authors

Correspondence to Guglielmo Lanzani or Fabio Benfenati.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 1151 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ghezzi, D., Antognazza, M., Maccarone, R. et al. A polymer optoelectronic interface restores light sensitivity in blind rat retinas. Nature Photon 7, 400–406 (2013). https://doi.org/10.1038/nphoton.2013.34

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nphoton.2013.34

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing