昆虫视觉电生理技术研究进展

doi:10.13287/j.1001-9332.202403.032

摘要/Abstract

摘要： 昆虫视觉电生理技术是研究昆虫感光细胞和视觉神经元电学特性的重要技术,包括视网膜电位技术(ERG)和微电极细胞内记录技术(MIR)。ERG技术记录的是昆虫的视网膜对不同光刺激产生的电压或电流变化,这种反应发生在细胞外。MIR则是记录昆虫的单个感光细胞或视觉神经元对不同光刺激产生的电压或电流变化,这种反应发生在细胞内。昆虫电生理技术有助于探究昆虫视觉对光的电生理响应机制和明确昆虫敏感光谱和光感受器类型。本文介绍了ERG和MIR的基本结构及原理,总结了近20年来两种技术在昆虫感光电生理方面的应用,可为阐明昆虫对光的感受机制以及利用昆虫的趋光性防治害虫提供参考。

关键词: 视网膜电位, 微电极细胞内记录, 敏感光谱, 光感受器

Abstract: Insect visual electrophysiological techniques are important to study the electrical characteristics of photoreceptor cells and visual neurons in insects, including electroretinography (ERG) and microelectrode intracellular recording (MIR). ERG records the changes of voltage or electric current in the retina of insects in response to different light stimuli, which occurs outside the cell. MIR records the changes in individual photoreceptor cells or visual neurons of an insect exposed to different lights, which occurs inside the cell. Insect visual electrophysiological techniques can explore the mechanism of electrophysiological response of insects’ vision to light and reveal their sensitive light spectra and photoreceptor types. This review introduced the basic structure and the principle of ERG and MIR, and summarized their applications in insect researches in the past 20 years, which would provide references for elucidating the mechanism of light perception in insects and the use of insect phototropism to control pests.

Key words: electroretinography, microelectrode intracellular recording, sensitive light spectra, photoreceptor

刘航, 魏成梅, 冯太阳, 董文霞, 肖春. 昆虫视觉电生理技术研究进展[J]. 应用生态学报, 2024, 35(3): 858-866.

LIU Hang, WEI Chengmei, FENG Taiyang, DONG Wenxia, XIAO Chun. Research progress on insect visual electrophysiological techniques[J]. Chinese Journal of Applied Ecology, 2024, 35(3): 858-866.

参考文献

[1] Stalleicken J, Labhart T, Mouritsen H. Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. Journal of Comparative Physiology, 2006, 192: 321-331
[2] Jia LP, Liang AP. Fine structure of the compound eyes of Callitettix versicolor (Insecta: Hemiptera). Annals of the Entomological Society of America, 2015, 108: 316-324
[3] Montell C. Visual transduction in drosophila. Annual Review of Cell and Developmental Biology, 1999, 15: 231-268
[4] Song BM, Lee CH. Toward a mechanistic understanding of color vision in insects. Frontiers in Neural Circuits, 2018, 12: 1-9
[5] 唐加菜, 魏成梅, 赵婧, 等. 昆虫单个感觉器记录技术研究进展. 应用生态学报, 2022, 33(11): 3146-3158
[6] Roeder KD. Synchronized activity in the optic and protocerebral ganglia of the grasshopper, Melanoplus femur-rubrum. Journal of Cellular Physiology, 1939, 14: 299-307
[7] 刘育民. 美洲大蠊电反应研究. 生理学报, 1964, 27(30): 232-240
[8] 刘育民, 李朝义, 陈德茂. 昆虫重叠象复眼的视网膜电图. 科学通报, 1966, 17(8): 361-363
[9] 刘育民, 陈德茂, 李朝义. 家蝇复眼和视叶综合电反应的分析. 生理学报, 1980, 32 (1): 68-78
[10] 郭爱克. 丽蝇光感受特性的研究. 中国科学, 1980, 9(1): 907-913
[11] Eisuke E, Kiyoko W, Takahiko H, et al. A comparison of electrophysiologically determined spectral responses in 35 species of lepidoptera. Journal of Insect Physiology, 1982, 28: 675-682
[12] Paulk AC, Dacks AM, Fellous JM, et al. Visual processing in the central bee brain. Journal of Neuroscience, 2009, 29: 9987-9999
[13] Peron S, Gabbiani F. Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nature Neuroscience, 2009, 12: 318-326
[14] Ogawa Y. The Physiological Basis for Color Vision in the Eastern Pale Clouded Yellow Butterfly, Colias erate. PhD Thesis. Kanagawa, Japan: The Graduate University for Advanced Studies, 2013
[15] Francismeire JT, Olle L, Miriam JH, et al. Out of the blue: The spectral sensitivity of hummingbird hawkmoths. Journal of Comparative Physiology A, 2014, 200: 537-546
[16] Mcneill CA, Allan SA, Koehler PG, et al. Vision in the common bed bug Cimex lectularius L. (Hemiptera: Cimicidae): Eye morphology and spectral sensitivity. Medical & Veterinary Entomology, 2016, 30: 426-434
[17] Guignard Q, Spaethe J, Slippers B. Evidence for UV-green dichromacy in the basal hymenopteran Sirex nocti-lio (Siricidae). Scientific Reports, 2021, 11: 1-10
[18] Annette S, Sarah M, Elke B, et al. Electrophysiology meets ecology: Investigating how vision is tuned to the life style of an animal using electroretinography. Journal of Undergraduate Neuroscience Education, 2015, 13: A234-A243
[19] 刘军和, 赵紫华. 昆虫视觉在寄主寻找及定位过程中的作用. 植物保护学报, 2017, 44(3): 353-362
[20] Daniel T, Berón AM, Julieta S. Identification of individual neurons reflecting short and long-term visual memory in an arthropod. Journal of Neuroscience, 2003, 23: 8539-8546
[21] Martínez HJ, Vorobyev M, Schorn J, et al. Evidence of red sensitive photoreceptors in Pygopleurus israelitus (Glaphyridae: Coleoptera) and its implications for beetle pollination in the southeast Mediterranean. Journal of Comparative Physiology A, 2012, 198: 451-463
[22] Knox BE, Ernesto S, Katherine M, et al. Heterologous expression of Limulus rhodopsin. Journal of Biological Chemistry, 2003, 278: 493-502
[23] Salcedo E, Zheng L, Phistry M, et al. Molecular basis for ultraviolet vision in invertebrates. Journal of Neuroscience, 2003, 23: 873-878
[24] Cronin TW, Jarvilehto M, Weckstrom M, et al. Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae). Journal of Comparative Physiology, 2000, 186: 1-12
[25] Arikawa K, Mizuno S, Kinoshita M, et al. Coexpression of two visual pigments in a photoreceptor causes an abnormally broad spectral sensitivity in the eye of the butterfly Papilio xuthus. Journal of Neuroscience Research, 2003, 23: 4527-4532
[26] Song BM, Lee CH. Toward a mechanistic understanding of color vision in insects. Frontiers in Neural Circuits, 2018. 12: 16-25
[27] Skorupski P, Doring TF, Chittka L. Photoreceptor spectral sensitivity in island and mainland populations of the bumblebee, Bombus terrestris. Journal of Comparative Physiology A, 2007, 193: 485-494
[28] Skorupski P, Chittka L. Photoreceptor processing speed and input resistance changes during light adaptation correlate with spectral class in the bumblebee, Bombus impatiens. PLoS One, 2011, 6: 1-8
[29] Yang EC, Lin HC, Hung YS. Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. Journal of Insect Physiology, 2004, 50: 913-925
[30] Rosner R, Homberg U. Widespread sensitivity to looming stimuli and small moving objects in the central complex of an insect brain. Journal of Neuroscience, 2013, 33: 8122-8133
[31] Trager U, Homberg U. Polarization-sensitive descending neurons in the locust: connecting the brain to thoracic ganglia. Journal of Neuroscience, 2011, 31: 2238-2247
[32] McCulloch KJ, Osorio D, Briscoe AD. Determination of photoreceptor cell spectral sensitivity in an insect model from in vivo intracellular recordings. Journal of Visualized Experiments, 2016, 108: 1-14
[33] Kirchner SM, Döring TF, Saucke H. Evidence for trichromacy in the green peach aphid, Myzus persicae (Hemiptera: Aphididae). Journal of Insect Physiology, 2005, 51: 1255-1260
[34] Döring TF, Kirchner SM, Skorupski P, et al. Spectral sensitivity of the green photoreceptor of winged pea aphids. Physiological Entomology, 2011, 36: 392-396
[35] Kentaro A, Motohiro W, Xudong Q, et al. Sexual dimorphism of short-wavelength photoreceptors in the small white butterfly, Pieris rapae crucivora. Journal of Neuroscience, 2005, 25: 5935-5942
[36] Wakakuwa M, Stavenga DG, Arikawa K. Spectral organization of ommatidia in flower-visiting insects. Photochemistry and Photobiology, 2007, 83: 27-34
[37] Arikawa K. Spectral organization of the eye of a butterfly Papilio. Journal of Comparative Physiology, 2003, 189: 791-800
[38] Arikawa K. The eyes and vision of butterflies. Journal of Physiology, 2017, 596: 5457-5464
[39] Koshitaka H, Kinoshita M, Vorobyev M, et al. Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proceedings of the Royal Society B: Biological Sciences, 2008, 275: 947-954
[40] Echen PJ, Eawata H, Earikawa AK, et al. Extreme spectral richness in the eye of the common bluebottle butterfly, Graphium sarpedon. Frontiers in Physiology, 2016, 4: 1-12
[41] Kelber A. Receptor based models for spontaneous colour choices in flies and butterflies. Entomologia Experimentalis et Applicata, 2010, 99: 231-244
[42] 魏国树, 张青文, 周明牂, 等. 棉铃虫蛾复眼光反应特性. 昆虫学报, 2002, 45(3): 323-328
[43] Belušic G, Šporar K, Meglic A. Extreme polarisation sensitivity in the retina of the corn borer moth Ostrinia. Journal of Experimental Biology, 2017, 220: 2047-2056
[44] Crook DJ, Hull-Sanders HM, Hibbard EL, et al. A comparison of electrophysiologically determined spectral responses in six subspecies of Lymantria. Journal of Economic Entomology, 2014, 107: 667-674
[45] Satoh A, Stewart FJ, Koshitaka H, et al. Redshift of spectral sensitivity due to screening pigment migration in the eyes of a moth, Adoxophyes orana. Zoological Letters, 2017, 3: 1-11
[46] Jakobsson J, Henze MJ, Svensson GP, et al. Visual cues of oviposition sites and spectral sensitivity of Cydia strobilella L. Journal of Insect Physiology, 2017, 101: 1-23
[47] Crook DJ, Chiesa SG, Warden ML, et al. Electrophysiologically determined spectral responses in Lobesia botrana (Lepidoptera: Tortricidae). Journal of Economic Entomology, 2022, 115: 1499-1504
[48] Martinez-Harms J, Palacios AG, Marquez N, et al. Can red flowers be conspicuous to bees? Bombus dahlbomii and South American temperate forest flowers as a case in point. Journal of Experimental Biology, 2010, 213: 564-571
[49] Skorupski P, Chittka L. Photoreceptor spectral sensitivity in the bumblebee, Bombus impatiens (Hymenoptera: Apidae). PLoS One, 2010, 5: 1-5
[50] Kooi CJVD, Stavenga DG, Arikawa K. Evolution of insect color vision: From spectral sensitivity to visual ecology. Annual Review of Entomology, 2021, 66: 435-461
[51] Camlitepe Y, Aksoy V, Uren N, et al. An experimental analysis on the magnetic field sensitivity of the black-meadow ant Formica pratensis Retzius (Hymenoptera: Formicidae). Acta Biologica Hungarica, 2005, 56: 215-224
[52] Aksoy V. Experience based use of landmark and vector based orientation during homing by the ant Formica cunicularia (Hymenoptera: Formicidae). Journal of Insect Behavior, 2014, 27: 357-369
[53] Aksoy V, Camlitepe Y. Abehavioral analysis of achromatic cue perception by the ant Cataglyphis aenescens (Hymenoptera; Formicidae). Turkish Journal of Zoology, 2014, 38: 199-208
[54] Jiang YL, Guo YY, Wu YQ, et al. Spectral sensitivity of the compound eyes of Anomala corpulenta Motschulsky (Coleoptera: Scarabaeoidea). Journal of Integrative Agriculture, 2015, 14: 706-713
[55] Tokushima Y, Uehara T, Yamaguchi T, et al. Broadband photoreceptors are involved in violet light preference in the parasitoid fly Exorista japonica. PLoS One, 2016, 11: 160-170
[56] Sándor K, András G, József F, et al. In search of the spectral composition of an effective light trap for the mushroom pest Lycoriella ingenua (Diptera: Sciaridae). Scientific Reports, 2021, 11: 220-229
[57] Hu X, Leming MT, Metoxen AJ, et al. Light-mediated control of rhodopsin movement in mosquito photoreceptors. Journal of Neuroscience, 2012, 32: 13661-13667
[58] Döring TF, Skorupski P. Host and nonhost leaves in the colour space of the colorado potato beetle (Coleoptera: Chrysomelidae). Entomologia Generalis, 2007, 29: 81-95
[59] Crook DJ, Francese JA, Zylstra KE, et al. Laboratory and field response of the emerald ash borer (Coleoptera: Buprestidae), to selected regions of the electromagnetic spectrum. Journal of Economic Entomology, 2009, 102: 2160-2169
[60] 陈晓霞, 闫海燕, 魏玮. 光谱和光强度对龟纹瓢虫成虫趋光行为的影响. 生态学报. 2009, 29(5): 2349-2355
[61] Ogawa Y, Falkowski M, Narendra A, et al. Three spectrally distinct photoreceptors in diurnal and nocturnal Australian ants. Proceedings of the Royal Society B, 2015, 282: 1-7
[62] 杨小凡, 魏国树, 马爱红, 等. 昆虫紫外视觉研究进展. 植物保护学报, 2022, 49(1): 131-145
[63] Matsumoto Y, Wakakuwa M, Matsunaga S, et al. Physiological basis of phototaxis to near-infrared light in Nephotettix cincticeps. Journal of Comparative Physiology A, 2014, 200: 527-536
[64] Schmeling F, Wakakuwa M, Tegtmeier J. Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust, Schistocerca gregaria. Journal of Experimental Biology, 2014, 217: 3557-3568
[65] Futahashi R, Kawahara-Miki R, Kinoshita M, et al. Extraordinary diversity of visual opsin genes in dragonflies. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112: 1247-1256
[66] 闫海霞, 魏国树, 吴卫国, 等. 中华通草蛉复眼光感受性. 昆虫学报, 2007, 50(11): 1099-1104
[67] Kishi M, Wakakuwa M, Kansako M, et al. Action spectrum of phototactic behavior and compound eye spectral sensitivity in the yellow tea thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae). Japanese Journal of Applied Entomology and Zoology, 2014, 58: 13-16
[68] Francismeire JT, Kelber A, Rodríguez-Gironés MA. Wavelength discrimination in the hummingbird hawkmoth Macroglossum stellatarum. Journal of Experimental Biology, 2016, 219: 553-560
[69] Honkanen A, Immonen EV, Salmela I, et al. Insect photoreceptor adaptations to night vision. Philosophical Transactions of the Royal Society B, 2017, 372: 1-9
[70] Kelber A, Balkenius A, Warrant EJ. Scotopic colour vision in nocturnal hawkmoths. Nature, 2002, 419: 922-925
[71] Gecear RJ, Laverty TM. Flower constancy in bumblebees: A test of the trait variability hypothesis. Animal Behaviour, 2005, 69: 939-949.
[72] Casper J, Ollerton J. The origins of flowering plants and animal pollination. Science, 2020, 368: 1-7
[73] Wehner R, Muller M. The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103: 575-579
[74] Graham P, Cheng K. Which portion of the natural panorama is used for view-based navigation in the Australian desert ant? Journal of Comparative Physiology A, 2009, 195: 681-689
[75] Webb MB. Spontaneous formation of multiple routes in individual desert ants (Cataglyphis velox). Behavioral Ecology, 2012, 23: 944-954
[76] Narendra A, Reid SF, Raderschall CA. Navigational efficiency of nocturnal Myrmecia ants suffers at low light levels. PLoS One, 2013, 8: 1-7
[77] Zeil J, Narendra A, Sturzl W. Looking and homing: How displaced ants decide where to go. Philosophical Transactions of the Royal Society B, 2014, 369: 1-14
[78] Kinoshita M, Stewart FJ, Ômura H. Multisensory integration in Lepidoptera: Insights into flower-visitor interactions. BioEssays, 2017, 39: 1-11
[79] Lunau K, Maier EJ. Innate colour preferences of flower visitors. Journal of Comparative Physiology A, 1995, 177: 1-19
[80] Streinzer M, Roth N, Paulus HF, et al. Color preference and spatial distribution of glaphyrid beetles suggest a key role in the maintenance of the color polymorphism in the peacock anemone (Anemone pavonina Ranunculaceae) in Northern Greece. Journal of Comparative Physiology A, 2019, 205: 735-743
[81] Kooi CJVD, Dyer AG, Kevan PG, et al. Functional Significance of the Optical Properties of Flowers for Visual Signalling. Oxford: Oxford University Press, 2019
[82] Mcculloch KJ, Osorio D, Briscoe AD. Sexual dimorphism in the compound eye of Heliconius erato: A nymphalid butterfly with at least five spectral classes of photoreceptor. Journal of Experimental Biology, 2016, 219: 2377-2387
[83] Chen PJ, Arikawa K, Yang EC. Diversity of the photoreceptors and spectral opponency in the compound eye of the golden birdwing, Troides aeacus formosanus. PLoS One, 2013, 8: 1-10
[84] Wakakuwa M, Stavenga DG, Kurasawa M, et al. A unique visual pigment expressed in green, red and deep-red receptors in the eye of the small white butterfly, Pieris rapae crucivora. Journal of Experimental Biology, 2004, 207: 2803-2810
[85] Pirih P, Arikawa K, Stavenga DG. An expanded set of photoreceptors in the eastern pale clouded yellow butterfly, Colias erate. Journal of Comparative Physiology A, 2010, 196: 501-517
[86] Nagloo N, Kinoshita M, Arikawa K. Spectral organization of the compound eye of a migrating nymphalid, the chestnut tiger butterfly Parantica sita. Journal of Experimental Biology, 2020, 223: 1-9
[87] Yamaguchi S, Desplan C, Heisenberg M. Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 2010, 107: 5634-5639
[88] Sarah N, Yuri O, Karin N. Dual receptive fields underlying target and wide-field motion sensitivity in looming-sensitive descending neurons. eNeuro, 2023, 10: 1-15
[89] Döring TF, Kirchner SM, Skorupski P, et al. Spectral sensitivity of the green photoreceptor of winged pea aphids. Physiological Entomology, 2011, 36: 392-396
[90] Ogawa Y, Falkowski M, Narendra A, et al. Three spectrally distinct photoreceptors in diurnal and nocturnal Australian ants. Proceedings of the Royal Society B: Biological Sciences, 2015, 282: 1-7
[91] Ilić M, Pirih P, Belušic G. Four photoreceptor classes in the open rhabdom eye of the red palm weevil, Rynchophorus ferrugineus Olivier. Journal of Comparative Physiology A, 2016, 202: 203-213
[92] Maksimovic S, Layne JE, Buschbeck EK. Spectral sensitivity of the principal eyes of sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae), larvae. Journal of Experimental Biology, 2011, 214: 3524-3531
[93] Saari P, Immonen EV, French AS, et al. Electrical interactions between photoreceptors in the compound eye of Periplaneta americana. Journal of Experimental Biology, 2018, 221: 1-24
[94] Frederiksen R, Wcislo WT, Warrant EJ. Visual reliability and information rate in the retina of a nocturnal bee. Current Biology, 2008, 18: 349-353.
[95] Heimonen K, Salmela I, Kontiokari P, et al. Larger functional variability in cockroach photoreceptors: Optimizationto low light levels. Journal of Neurosience, 2006, 2: 13454-13462
[96] Pirhofer WK, Warrant EJ, Barth FG. Adaptations for vision in dim light: Impulse responses and bumps in nocturnal spider photoreceptors cells (Cupiennius salei Keys). Journal of Comparative Physiology A, 2007, 193: 1081-1087
[97] Sharkey CR, Blanco J, Leibowitz MM, et al. The spectral sensitivity of Drosophila photoreceptors. Scientific Reports, 2020, 10: 1-13
[98] Juusola MI, Dau A, Zheng L, et al. Electrophysiological method for recording intracellular voltage responses of drosophila photoreceptors and interneurons to light stimuli in vivo. Journal of Visualized Experiments, 2016,112: 1-16
[99] Hardie RC, Postma M. Phototransduction in microvillar photoreceptors of Drosophila and other invertebrates// Fritzsch B, ed. The Senses: A Comprehensive Reference. New York: Academic Press, 2021: 77-130
[100] Song Z, Marten P, Stephen A, et al. Stochastic, adaptive sampling of information by microvilli in fly photoreceptors. Current Biology, 2012, 22: 1371-1380
[101] Fu Q, Wang H, Hu C, et al. Towards computational models and applications of insect visual systems for motion perception: A review. Artificial Life, 2019, 25: 263-311
[102] 李伟红, 暴学祥. 昆虫脑中蕈形体功能的研究进展. 淮海工学院学报: 自然科学版, 2003, 12(4): 55-58
[103] Kinoshita M, Shimohigasshi M, Tominaga Y, et al. Topographically distinct visual and olfactory inputs to the mushroom body in the swallowtail butterfly, Papilio xuthus. Journal of Comparative Neurology, 2014, 523: 162-182