Neuroscience Bulletin

, Volume 32, Issue 3, pp 246–252 | Cite as

Biophotons Contribute to Retinal Dark Noise

Report

Abstract

The discovery of dark noise in retinal photoreceptors resulted in a long-lasting controversy over its origin and the underlying mechanisms. Here, we used a novel ultra-weak biophoton imaging system (UBIS) to detect biophotonic activity (emission) under dark conditions in rat and bullfrog (Rana catesbeiana) retinas in vitro. We found a significant temperature-dependent increase in biophotonic activity that was completely blocked either by removing intracellular and extracellular Ca2+ together or inhibiting phosphodiesterase 6. These findings suggest that the photon-like component of discrete dark noise may not be caused by a direct contribution of the thermal activation of rhodopsin, but rather by an indirect thermal induction of biophotonic activity, which then activates the retinal chromophore of rhodopsin. Therefore, this study suggests a possible solution regarding the thermal activation energy barrier for discrete dark noise, which has been debated for almost half a century.

Keywords

Biophoton Rat and bullfrog retinas Retinal dark noise Phosphodiesterase 6 Ca2+ Biophoton imaging 

References

  1. 1.
    Baylor DA, Matthews G, Yau KW. Two components of electrical dark noise in toad retinal rod outer segments. The Journal of Physiology 1980, 309: 591–621.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Rieke F, Baylor DA. Molecular origin of continuous dark noise in rod photoreceptors. Biophysical Journal 1996, 71: 2553–2572.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Barlow RB, Birge RR, Kaplan E, Tallent JR. On the molecular origin of photoreceptor noise. Nature 1993, 366: 64–66.CrossRefPubMedGoogle Scholar
  4. 4.
    Liu J, Liu MY, Nguyen JB, Bhagat A, Mooney V, Yan EC. Thermal decay of rhodopsin: role of hydrogen bonds in thermal isomerization of 11-cis retinal in the binding site and hydrolysis of protonated Schiff base. Journal of the American Chemical Society 2009, 131: 8750–8751.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Liu J, Liu MY, Nguyen JB, Bhagat A, Mooney V, Yan EC. Thermal properties of rhodopsin: insight into the molecular mechanism of dim-light vision. The Journal of Biological Chemistry 2011, 286: 27622–27629.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Lorenz-Fonfria VA, Furutani Y, Ota T, Ido K, Kandori H. Protein fluctuations as the possible origin of the thermal activation of rod photoreceptors in the dark. Journal of the American Chemical Society 2010, 132: 5693–5703.CrossRefPubMedGoogle Scholar
  7. 7.
    Kukura P, McCamant DW, Yoon S, Wandschneider DB, Mathies RA. Structural observation of the primary isomerization in vision with femtosecond-stimulated Raman. Science 2005, 310: 1006–1009.CrossRefPubMedGoogle Scholar
  8. 8.
    Gozem S, Schapiro I, Ferre N, Olivucci M. The molecular mechanism of thermal noise in rod photoreceptors. Science 2012, 337: 1225–1228.CrossRefPubMedGoogle Scholar
  9. 9.
    Ala-Laurila P, Donner K, Koskelainen A. Thermal activation and photoactivation of visual pigments. Biophysical Journal 2004, 86: 3653–3662.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Luo DG, Yue WW, Ala-Laurila P, Yau KW. Activation of visual pigments by light and heat. Science 2011, 332: 1307–1312.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Khrenova MG, Bochenkova AV, Nemukhin AV. Modeling reaction routes from rhodopsin to bathorhodopsin. Proteins 2010, 78: 614–622.PubMedGoogle Scholar
  12. 12.
    Barlow HB. Purkinje shift and retinal noise. Nature 1957, 179: 255–256.CrossRefPubMedGoogle Scholar
  13. 13.
    Ala-Laurila P, Pahlberg J, Koskelainen A, Donner K. On the relation between the photoactivation energy and the absorbance spectrum of visual pigments. Vision Research 2004, 44: 2153–2158.CrossRefPubMedGoogle Scholar
  14. 14.
    Cohen S, Popp FA. Biophoton emission of human body. Indian Journal of Experimental Biology 2003, 41: 440–445.PubMedGoogle Scholar
  15. 15.
    Albrecht-Buehler G. Rudimentary form of cellular “vision”. Proceedings of the National Academy of Sciences of the United States of America 1992, 89: 8288–8292.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Farhadi A, Forsyth C, Banan A, Shaikh M, Engen P, Fields JZ, et al. Evidence for non-chemical, non-electrical intercellular signaling in intestinal epithelial cells. Bioelectrochemistry 2007, 71: 142–148.CrossRefPubMedGoogle Scholar
  17. 17.
    Fels D. Cellular communication through light. PloS One 2009, 4: e5086.CrossRefPubMedGoogle Scholar
  18. 18.
    Sun Y, Wang C, Dai J. Biophotons as neural communication signals demonstrated by in situ biophoton autography. Photochemical and Photobiological Sciences 2010, 9: 315–322.CrossRefGoogle Scholar
  19. 19.
    Tang R, Dai J. Spatiotemporal imaging of glutamate-induced biophotonic activities and transmission in neural circuits. PloS One 2014, 9: e85643.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Tang R, Dai J. Biophoton signal transmission and processing in the brain. Journal of Photochemistry and Photobiology B, Biology 2014, 139: 71–75.CrossRefPubMedGoogle Scholar
  21. 21.
    Mayhew TM, Astle D. Photoreceptor number and outer segment disk membrane surface area in the retina of the rat: stereological data for whole organ and average photoreceptor cell. Journal of Neurocytology 1997, 26: 53–61.CrossRefPubMedGoogle Scholar
  22. 22.
    Zhang YD, Straznicky C. The morphology and distribution of photoreceptors in the retina of Bufo marinus. Anatomy and Embryology 1991, 183: 97–104.CrossRefPubMedGoogle Scholar
  23. 23.
    Holcman D, Korenbrot JI. The limit of photoreceptor sensitivity: molecular mechanisms of dark noise in retinal cones. The Journal of General Physiology 2005, 125: 641–660.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Katz B, Minke B. Phospholipase C-mediated suppression of dark noise enables single-photon detection in Drosophila photoreceptors. The Journal of Neuroscience 2012, 32: 2722–2733.CrossRefGoogle Scholar
  25. 25.
    Yamazaki A, Moskvin O, Yamazaki RK. Phosphorylation by cyclin-dependent protein kinase 5 of the regulatory subunit (Pgamma) of retinal cgmp phosphodiesterase (PDE6): its implications in phototransduction. Advances in Experimental Medicine and Biology 2002, 514: 131–153.CrossRefPubMedGoogle Scholar
  26. 26.
    Baylor DA, Matthews G, Yau KW. Temperature effects on the membrane current of retinal rods of the toad. The Journal of Physiology 1983, 337: 723–734.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Ala-Laurila P, Albert RJ, Saarinen P, Koskelainen A, Donner K. The thermal contribution to photoactivation in A2 visual pigments studied by temperature effects on spectral properties. Visual Neuroscience 2003, 20: 411–419.CrossRefPubMedGoogle Scholar
  28. 28.
    Benninger RK, Hao M, Piston DW. Multi-photon excitation imaging of dynamic processes in living cells and tissues. Reviews of Physiology, Biochemistry and Pharmacology 2008, 160: 71–92.PubMedGoogle Scholar
  29. 29.
    Perkins GA, Ellisman MH, Fox DA. Three-dimensional analysis of mouse rod and cone mitochondrial cristae architecture: bioenergetic and functional implications. Molecular Vision 2003, 9: 60–73.PubMedGoogle Scholar
  30. 30.
    Zhuravlev AI, Tsvylev OP, Zubkova SM. [Spontaneous endogenous ultraweak luminescence of rat liver mitochondria in conditions of normal metabolism]. Biofizika 1973, 18: 1037–1040.PubMedGoogle Scholar
  31. 31.
    Dotta BT, Buckner CA, Cameron D, Lafrenie RF, Persinger MA. Biophoton emissions from cell cultures: biochemical evidence for the plasma membrane as the primary source. General Physiology and Biophysics 2011, 30: 301–309.PubMedGoogle Scholar
  32. 32.
    Donner K, Firsov ML, Govardovskii VI. The frequency of isomerization-like ‘dark’ events in rhodopsin and porphyropsin rods of the bull-frog retina. The Journal of Physiology 1990, 428: 673–692.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Ala-Laurila P, Donner K, Crouch RK, Cornwall MC. Chromophore switch from 11-cis-dehydroretinal (A2) to 11-cis-retinal (A1) decreases dark noise in salamander red rods. The Journal of Physiology 2007, 585: 57–74.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer Science+Business Media Singapore 2016

Authors and Affiliations

  1. 1.Wuhan Institute for Neuroscience and NeuroengineeringSouth Central University for NationalitiesWuhanChina
  2. 2.Department of Neurobiology, College of Life SciencesSouth Central University for NationalitiesWuhanChina

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