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Neurons innervating the lamina in the butterfly, Papilio xuthus

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Abstract

The butterfly Papilio xuthus has compound eyes with three types of ommatidia. Each type houses nine spectrally heterogeneous photoreceptors (R1–R9) that are divided into six spectral classes: ultraviolet, violet, blue, green, red, and broad-band. Analysis of color discrimination has shown that P. xuthus uses the ultraviolet, blue, green, and red receptors for foraging. The ultraviolet and blue receptors are long visual fibers terminating in the medulla, whereas the green and red receptors are short visual fibers terminating in the lamina. This suggests that processing of wavelength information begins in the lamina in P. xuthus, unlike in flies. To establish the anatomical basis of color discrimination mechanisms, we examined neurons innervating the lamina by injecting Neurobiotin into this neuropil. We found that in addition to photoreceptors and lamina monopolar cells, three distinct groups of cells project fibers into the lamina. Their cell bodies are located (1) at the anterior rim of the medulla, (2) between the proximal surface of the medulla and lobula plate, and (3) in the medulla cell body rind. Neurobiotin injection also labeled distinct terminals in medulla layers 1, 2, 3, 4 and 5. Terminals in layer 4 belong to the long visual fibers (R1, 2 and 9), while arbors in layers 1, 2 and 3 probably correspond to terminals of three subtypes of lamina monopolar cells, respectively. Immunocytochemistry coupled with Neurobiotin injection revealed their transmitter candidates; neurons in (1) and a subset of neurons in (2) are immunoreactive to anti-serotonin and anti-γ-aminobutyric acid, respectively.

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Abbreviations

5-HT:

5-Hydroxytryptamine (serotonin)

GABA:

γ-Aminobutyric acid

LMC:

Lamina monopolar cell

lvf:

Long visual fiber

svf:

Short visual fiber

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Acknowledgments

We thank Dr. Uwe Homberg and Dr. Finlay Stewart for critically reading the manuscript. This work was supported in part by the JSPS Grants-in-Aid for Scientific Research No. 21247009 to KA, No. 24570084 to MK, the MAFF (Ministry of Agriculture, Forestry and Fisheries of Japan) grant (Elucidation of biological mechanisms of photoresponse and development of advanced technologies utilizing light) No. INSECT-1101 to KA. All experiments were conducted according to the MEXT (Ministry of Education, Culture, Sports, Science and Technology of Japan) guidelines for proper conduct of animal experiments and related activities in academic research institutions.

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  1. Laboratory of Neuroethology, Sokendai-Hayama (The Graduate University for Advanced Studies), Shonan Village, Hayama, Kanagawa, 240-0193, Japan

    Yoshitaka Hamanaka, Hiromichi Shibasaki, Michiyo Kinoshita & Kentaro Arikawa

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  1. Yoshitaka Hamanaka
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  2. Hiromichi Shibasaki
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  3. Michiyo Kinoshita
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  4. Kentaro Arikawa
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Correspondence to Kentaro Arikawa.

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Hamanaka, Y., Shibasaki, H., Kinoshita, M. et al. Neurons innervating the lamina in the butterfly, Papilio xuthus . J Comp Physiol A 199, 341–351 (2013). https://doi.org/10.1007/s00359-013-0798-6

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  • DOI: https://doi.org/10.1007/s00359-013-0798-6

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