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

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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.

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Notes

  1. Note that the abbreviation, dist-G, contains both ‘double-peaked green (dG)’ and ‘single-peaked green (sG)’ spectral classes in the distal tier in our previous publications (Arikawa et al. 1999). The B class in the current study contains both narrow-B and broad-B receptor subclasses described in Kinoshita et al. (2006).

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

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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.

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Authors and Affiliations

  1. Laboratory of Neuroethology, SOKENDAI (The Graduate University for Advanced Studies), Hayama, Japan

    Masashi Kawasaki, Michiyo Kinoshita & Kentaro Arikawa

  2. Department of Biology, University of Virginia, Charlottesville, VA, 22904, USA

    Masashi Kawasaki

  3. Centre for Molecular Materials, Biophysics, University of Oulu, Oulu, Finland

    Matti Weckström

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  1. Masashi Kawasaki
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  2. Michiyo Kinoshita
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  3. Matti Weckström
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  4. Kentaro Arikawa
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Correspondence to Masashi Kawasaki.

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Kawasaki, M., Kinoshita, M., Weckström, M. et al. Difference in dynamic properties of photoreceptors in a butterfly, Papilio xuthus: possible segregation of motion and color processing. J Comp Physiol A 201, 1115–1123 (2015). https://doi.org/10.1007/s00359-015-1039-y

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  • DOI: https://doi.org/10.1007/s00359-015-1039-y

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