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Human infrared vision is triggered by two-photon chromophore isomerization

  1. Krzysztof Palczewskie,2
  1. aDepartment of Medical Devices, Polgenix, Inc., Cleveland, OH 44106;
  2. bOphthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, MO 63110;
  3. cFaculty of Physics, Astronomy and Informatics, Institute of Physics, Nicolaus Copernicus University, 87-100 Torun, Poland;
  4. dDepartment of Chemistry and Biochemistry, University of Bern, CH-3012 Bern, Switzerland;
  5. eDepartment of Pharmacology, Cleveland Center for Membrane and Structural Biology, School of Medicine, Case Western Reserve University, Cleveland, OH 44106; and
  6. fDepartment of Chemistry and Centre for Theoretical and Computational Chemistry, University of Oslo, N-0315 Oslo, Norway

  1. Edited by Austin Roorda, University of California, Berkeley, CA, and accepted by the Editorial Board October 30, 2014 (received for review June 3, 2014)

Significance

This study resolves a long-standing question about the ability of humans to perceive near infrared radiation (IR) and identifies a mechanism driving human IR vision. A few previous reports and our expanded psychophysical studies here reveal that humans can detect IR at wavelengths longer than 1,000 nm and perceive it as visible light, a finding that has not received a satisfactory physical explanation. We show that IR light activates photoreceptors through a nonlinear optical process. IR light also caused photoisomerization of purified pigments and a model chromophore compound. These observations are consistent with our quantum mechanical model for the energetics of two-photon activation of rhodopsin. Thus, humans can perceive IR light via two-photon isomerization of visual pigment chromophores.

Abstract

Vision relies on photoactivation of visual pigments in rod and cone photoreceptor cells of the retina. The human eye structure and the absorption spectra of pigments limit our visual perception of light. Our visual perception is most responsive to stimulating light in the 400- to 720-nm (visible) range. First, we demonstrate by psychophysical experiments that humans can perceive infrared laser emission as visible light. Moreover, we show that mammalian photoreceptors can be directly activated by near infrared light with a sensitivity that paradoxically increases at wavelengths above 900 nm, and display quadratic dependence on laser power, indicating a nonlinear optical process. Biochemical experiments with rhodopsin, cone visual pigments, and a chromophore model compound 11-cis-retinyl-propylamine Schiff base demonstrate the direct isomerization of visual chromophore by a two-photon chromophore isomerization. Indeed, quantum mechanics modeling indicates the feasibility of this mechanism. Together, these findings clearly show that human visual perception of near infrared light occurs by two-photon isomerization of visual pigments.

Footnotes

  • ↵1G.P., F.V., and P.S. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: michele.cascella{at}kjemi.uio.no, max{at}fizyka.umk.pl, kefalov{at}vision.wustl.edu, or kxp65{at}case.edu.

  • Author contributions: G.P., F.V., P.S., M.P.B., D.S., K.K., M.C., M.W., V.J.K., and K.P. designed research; G.P., F.V., P.S., M.P.B., D.S., K.K., J.Z., M.C., and V.J.K. performed research; J.Z. contributed new reagents/analytic tools; G.P., P.S., M.P.B., D.S., K.K., J.Z., M.C., M.W., V.J.K., and K.P. analyzed data; and G.P., F.V., D.S., K.K., M.C., M.W., V.J.K., and K.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. A.R. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1410162111/-/DCSupplemental.

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