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Journal of Comparative Physiology A

, Volume 201, Issue 12, pp 1115–1123 | Cite as

Difference in dynamic properties of photoreceptors in a butterfly, Papilio xuthus: possible segregation of motion and color processing

  • Masashi KawasakiEmail author
  • Michiyo Kinoshita
  • Matti Weckström
  • Kentaro Arikawa
Original Paper

Abstract

The eyes of the Japanese yellow swallowtail butterfly, Papilio xuthus, contain six spectral classes of photoreceptors, each sensitive either in the ultraviolet, violet, blue, green, red or broadband wavelength regions. The green-sensitive receptors can be divided into two subtypes, distal and proximal. Previous behavioral and anatomical studies have indicated that the distal subtype appears to be involved in motion vision, while the proximal subtype is important for color vision. Here, we studied the dynamic properties of Papilio photoreceptors using light stimulation with randomly modulated intensity and light pulses. Frequency response (gain) of all photoreceptor classes shared a general profile—a broad peak around 10 Hz with a declining slope towards higher frequency range. At 100 Hz, the mean relative gain of the distal green receptors was significantly larger than any other receptor classes, indicating that they are the fastest. Photoreceptor activities under dim light were higher in the ultraviolet and violet receptors, suggesting higher transduction sensitivities. Responses to pulse stimuli also distinguished the green receptors from others by their shorter response latencies. We thus concluded that the distal green receptors carry high frequency information in the visual system of Papilio xuthus.

Keywords

Butterfly vision Motion vision Color vision Photoreceptor dynamics 

Abbreviations

B

blue

BB

broadband

G

green

dist-G

distal green

prox-G

proximal green

LED

light-emitting diode

R

red

UV

ultraviolet

V

violet

Notes

Acknowledgments

This work was supported by the SOKENDAI visiting professorship to MKa, the JSPS (Japanese Society for Promotion of Science) Grants-in-Aid for Scientific Research C to MKi (24570084) and A to KA (26251036), JSPS open partnership joint research project (Finland) to KA, the NARO (National Agriculture and Food Research Organization) grant for SIP (Strategic Innovation Promotion) Program “Technologies for creating next-generation agriculture, forestry and fisheries” to KA, and the research grant from the Academy of Finland (269332) to MW.

References

  1. Anderson J, Hardie RC (1996) Different photoreceptors within the same retina express unique combinations of potassium channels. J Comp Physiol A 178:513–522CrossRefGoogle Scholar
  2. Anderson JC, Laughlin SB (2000) Photoreceptor performance and the co-ordination of achromatic and chromatic inputs in the fly visual system. Vision Res 40:13–31CrossRefPubMedGoogle Scholar
  3. Arikawa K (2003) Spectral organization of the eye of a butterfly, Papilio. J Comp Physiol A 189:791–800CrossRefGoogle Scholar
  4. Arikawa K, Inokuma K, Eguchi E (1987) Pentachromatic visual system in a butterfly. Naturwissenschaften 74:297–298CrossRefGoogle Scholar
  5. Arikawa K, Mizuno S, Scholten DG, Kinoshita M, Seki T, Kitamoto J, Stavenga DG (1999) An ultraviolet absorbing pigment causes a narrow-band violet receptor and a single-peaked green receptor in the eye of the butterfly Papilio. Vision Res 39:1–8CrossRefPubMedGoogle Scholar
  6. Arikawa K, Mizuno S, Kinoshita M, Stavenga DG (2003) Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of a butterfly, Papilio xuthus. J Neurosci 23:4527–4532PubMedGoogle Scholar
  7. Bendat JS, Piersol AG (1971) Random data: analysis and measurement procedures. John Wiley and Sons Inc, New YorkGoogle Scholar
  8. Dyer AG, Arikawa K (2014) A hundred years of color studies in insects: with thanks to Karl von Frisch and the workers he inspired. J Comp Physiol A 200:409–410CrossRefGoogle Scholar
  9. Friedrich M, Wood EJ, Wu M (2011) Developmental evolution of the insect retina: insights from standardized numbering of homologous photoreceptors. J Exp Zool B 316:484–499CrossRefGoogle Scholar
  10. Frolov R, Immonen EV, Vähäsöyrinki M, Weckström M (2012) Postembryonic developmental changes in photoreceptors of the stick insect Carausius morosus enhance the shift to an adult nocturnal life-style. J Neurosci 32:16821–16831CrossRefPubMedGoogle Scholar
  11. Hardie RC (1985) Functional organization of the fly retina. In: Ottoson D (ed) Progress in Sensory Physiology, vol 5. Springer, Berlin Heidelberg New York Toronto, pp 1–79CrossRefGoogle Scholar
  12. He S, MacLeod DI (1997) Local nonlinearity in S-cones and their estimated light-collecting apertures. Vision Res 38:1001–1006CrossRefGoogle Scholar
  13. Heimonen K, Immonen EV, Frolov RV, Salmela I, Juusola M, Vähäsöyrinki M, Weckström M (2012) Signal coding in cockroach photoreceptors is tuned to dim environments. J Neurophysiol 108:2641–2652CrossRefPubMedGoogle Scholar
  14. Heisenberg M, Buchner E (1977) The role of retinula cell types in visual behavior of Drosophila melanogaster. J Comp Physiol A 117:127–162CrossRefGoogle Scholar
  15. Hodgkin A, Rushton W (1946) The electrical constants of a crustacean nerve fibre. Proc Roy Soc B 133:444–479CrossRefGoogle Scholar
  16. Horridge GA, Marčelja L, Jahnke R, Matič T (1983) Single electrode studies on the retina of the butterfly Papilio. J Comp Physiol A 150:271–294CrossRefGoogle Scholar
  17. Horridge GA, Marčelja L, Jahnke R (1984) Color vision in butterflies 1. Single colour experiments. J Comp Physiol A 155:529–542CrossRefGoogle Scholar
  18. Juusola M, de Polavieja GG (2003) The rate of information transfer of naturalistic stimulation by graded potentials. J Gen Physiol 122:191–206PubMedCentralCrossRefPubMedGoogle Scholar
  19. Juusola M, Kouvalainen E, Järvilehto M, Weckström M (1994) Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors. J Gen Physiol 104:593–621CrossRefPubMedGoogle Scholar
  20. Kaiser W (1975) The relationship between visual movement detection and colour vision in insects. In: Horridge GA (ed) The compound eye and vision in insects. Clarendon Press, Oxford, pp 359–377Google Scholar
  21. Kaiser PK, Boynton RM (ed) (1995) Human colour vision, 2nd edn. In. Optical Society of America, Washington DC, p 652Google Scholar
  22. Kinoshita M, Arikawa K (2014) Color and polarization vision in foraging Papilio. J Comp Physiol A 200:513–526CrossRefGoogle Scholar
  23. Kinoshita M, Kurihara D, Tsutaya A, Arikawa K (2006) Blue and double-peaked green receptors depend on ommatidial type in the eye of the Japanese yellow swallowtail Papilio xuthus. Zool Sci 23:199–204CrossRefPubMedGoogle Scholar
  24. Koch C (1998) Biophysics of computation: information processing in single neurons. Oxford University Press, Oxford, New York etcGoogle Scholar
  25. Koshitaka H, Kinoshita M, Vorobyev M, Arikawa K (2008) Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proc Roy Soc B 275:947–954CrossRefGoogle Scholar
  26. Kv Frisch (1914) Der Farbensinn und Formensinn der Biene. Zool Jb Physiol 37:1–238Google Scholar
  27. Land MF (1999) Motion and vision: why animals move their eyes. J Comp Physiol A 185:341–352CrossRefPubMedGoogle Scholar
  28. Laughlin S, Weckström M (1993) Fast and slow photoreceptors—a comparative study of the functional diversity of coding and conductances in the Diptera. J Comp Physiol A 172:593–609CrossRefGoogle Scholar
  29. Laughlin SB, van Steveninck RRD, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41CrossRefPubMedGoogle Scholar
  30. Lehrer M, Wehner R, Srinivasan M (1985) Visual scanning behavior in honeybees. J Comp Physiol A 157:405–415CrossRefPubMedGoogle Scholar
  31. Lehrer M, Wehner R, Srinivasan M (1989) How honeybees measure their distance from objects of unknown size. J Comp Physiol A 165:605–613CrossRefGoogle Scholar
  32. Livingstone M, Hubel D (1988) Segregation from color, movement, and depth—anatomy, physiology, and perception. Science 240:740–749CrossRefPubMedGoogle Scholar
  33. Marmarelis PZ, Marmarelis VZ (1978) Analysis of physiological systems : the white-noise approach. Plenum Press, New YorkCrossRefGoogle Scholar
  34. Schnaitmann C, Garbers C, Wachtler T, Tanimoto H (2013) Color discrimination with broadband photoreceptors. Curr Biol 23:2375–2382CrossRefPubMedGoogle Scholar
  35. Skorupski P, Chittka L (2010) Differences in photoreceptor processing speed for chromatic and achromatic vision in the bumblebee, Bombus terrestris. J Neurosci 30:3896–3903CrossRefPubMedGoogle Scholar
  36. Skorupski P, Chittka L (2011) Photoreceptor processing speed and input resistance changes during light adaptation correlate with spectral class in the bumblebee, Bombus impatiens. PLoS One 6:e25989PubMedCentralCrossRefPubMedGoogle Scholar
  37. Song Z, Postma M, Billings SA, Coca D, Hardie RC, Juusola M (2012) Stochastic, adaptive sampling of information by microvilli in fly photoreceptors. Curr Biol 22:1371–1380PubMedCentralCrossRefPubMedGoogle Scholar
  38. Srinivasan MV, Lehrer M (1984) Temporal acuity of honeybee vision: behavioural studies using moving stimuli. J Comp Physiol A 155:297–312CrossRefGoogle Scholar
  39. Strausfeld NJ, Lee J-K (1991) Neuronal basis for parallel visual processing in the fly. Vis Neurosci 7:13–33CrossRefPubMedGoogle Scholar
  40. Takemura SY, Arikawa K (2006) Ommatidial type-specific interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus. J Comp Neurol 494:663–672CrossRefPubMedGoogle Scholar
  41. Takemura S, Kinoshita M, Arikawa K (2005) Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus. J Comp Neurol 483:341–350CrossRefPubMedGoogle Scholar
  42. Vähäkainu A, Vähäsöyrinki M, Weckström M (2013) Membrane filtering properties of the bumblebee (Bombus terrestris) photoreceptors across three spectral classes. J Comp Physiol A 199:629–639CrossRefGoogle Scholar
  43. Van Hateren J, Laughlin S (1990) Membrane parameters, signal transmission, and the design of a graded potential neuron. J Comp Physiol A 166:437–448CrossRefPubMedGoogle Scholar
  44. Wakakuwa M, Kurasawa M, Giurfa M, Arikawa K (2005) Spectral heterogeneity of honeybee ommatidia. Naturwissenschaften 92:464–467CrossRefPubMedGoogle Scholar
  45. Wakakuwa M, Stavenga DG, Arikawa K (2007) Spectral organization of ommatidia in flower-visiting insects. Photochem Photobiol 83:27–34CrossRefPubMedGoogle Scholar
  46. Wardill TJ, List O, Li X, Dongre S, McCulloch M, Ting CY, O’Kane CJ, Tang S, Lee CH, Hardie RC, Juusola M (2012) Multiple spectral inputs improve motion discrimination in the Drosophila visual system. Science 336:925–931CrossRefPubMedGoogle Scholar
  47. Weckström M, Laughlin SB (1995) Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends Neurosci 18:17–21CrossRefPubMedGoogle Scholar
  48. Yamaguchi S, Wolf R, Desplan C, Heisenberg M (2008) Motion vision is independent of color in Drosophila. Proc Natl Acad Sci USA 105:4910–4915PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Masashi Kawasaki
    • 1
    • 2
    Email author
  • Michiyo Kinoshita
    • 1
  • Matti Weckström
    • 3
  • Kentaro Arikawa
    • 1
  1. 1.Laboratory of NeuroethologySOKENDAI (The Graduate University for Advanced Studies)HayamaJapan
  2. 2.Department of BiologyUniversity of VirginiaCharlottesvilleUSA
  3. 3.Centre for Molecular Materials, BiophysicsUniversity of OuluOuluFinland

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