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Morphological and electrophysiological specializations of photoreceptors in the love spot of hover fly Volucella pellucens

Published online by Cambridge University Press:  12 October 2021

Irina I. Ignatova ,
Ilkka Miinalainen  and
Roman V. Frolov Open the ORCID record for Roman V. Frolov [Opens in a new window]
Irina I. Ignatova
Affiliation:
Nano and Molecular Systems Research Unit, University of Oulu, Oulu, Finland
Ilkka Miinalainen
Affiliation:
Biocenter Tissue Imaging Center, University of Oulu, Oulu, Finland
Roman V. Frolov*
Affiliation:
Laboratory of Comparative Sensory Physiology, Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, Saint Petersburg, Russia
*
*Corresponding author: Roman V. Frolov, email: [email protected]
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Abstract

Studies of functional variability in the compound eyes of flies reveal superior temporal resolution of photoreceptors from the frontal areas that mediate binocular vision, and in males mate recognition and pursuit. However, the mechanisms underlying differences in performance are not known. Here, we investigated properties of hover fly Volucella pellucens photoreceptors from two regions of the retina, the frontal-dorsal “love spot” and the lateral one. Morphologically, the microvilli of the frontal-dorsal photoreceptors were relatively few in number per rhabdomere cross-section, short and narrow. In electrophysiological experiments involving stimulation with prolonged white-noise and natural time intensity series, frontal-dorsal photoreceptors demonstrated comparatively high corner frequencies and information rates. Investigation of possible mechanisms responsible for their superior performance revealed significant differences in the properties of quantum bumps, and, unexpectedly, relatively high absolute sensitivity of the frontal-dorsal photoreceptors. Analysis of light adaptation indicated that photoreceptors from two regions adapt similarly but because frontal-dorsal photoreceptors were depolarized much stronger by the same stimuli than the lateral photoreceptors, they reached a deeper state of adaptation associated with higher corner frequencies of light response. Recordings from the photoreceptor axons were characterized by spike-like events that can significantly expand the frequency response range. Seamless integration of spikes into the graded voltage responses was enabled by light adaptation mechanisms that accelerate kinetics and decrease duration of depolarizing light response transients.

Keywords

Volucella pellucensphotoreceptorquantum bumpssignal processingacute zonelight adaptation
Type
Research Article
Information
Visual Neuroscience , Volume 38 , 2021 , E015
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Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Beersma, D.G., Hoenders, B.J., Huiser, A.M. & Van, P. (1982). Refractive index of the fly rhabdomere. Journal of the Optical Society of America 72, 583–588.10.1364/JOSA.72.000583CrossRefGoogle ScholarPubMed
Belmonte, C. & Stensaas, L.J. (1975). Repetitive spikes in photoreceptor axons of the scorpion eye. Invertebrate eye structure and tetrodotoxin. The Journal of General Physiology 66, 649–655.10.1085/jgp.66.5.649CrossRefGoogle ScholarPubMed
Bendat, J.S. & Piersol, A.G. (1980). Engineering Applications of Correlation and Spectral Analysis. New York: Wiley.Google Scholar
Bendat, J.S. & Piersol, A.G. (2010). Data analysis. In Random Data: Analysis and Measurement Procedures, pp. 359–416. Hoboken: Wiley.10.1002/9781118032428CrossRefGoogle Scholar
Boschek, C.B. (1971). On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Zeitschrift für Zellforschung und Mikroskopische Anatomie 118, 369–409.10.1007/BF00331193CrossRefGoogle ScholarPubMed
Brandt, A. (2011). Noise and Vibration Analysis: Signal Analysis and Experimental Procedures. Chichester: Wiley.10.1002/9780470978160CrossRefGoogle Scholar
Burton, B.G. & Laughlin, S.B. (2003). Neural images of pursuit targets in the photoreceptor arrays of male and female houseflies Musca domestica. Journal of Experimental Biology 206, 3963–3977.10.1242/jeb.00600CrossRefGoogle ScholarPubMed
Burton, B.G., Tatler, B.W. & Laughlin, S.B. (2001). Variations in photoreceptor response dynamics across the fly retina. Journal of Neurophysiology 86, 950–960.10.1152/jn.2001.86.2.950CrossRefGoogle ScholarPubMed
Chu, B., Postma, M. & Hardie, R.C. (2013). Fractional Ca(2+) currents through Trp and Trpl channels in drosophila photoreceptors. Biophysical Journal 104, 1905–1916.10.1016/j.bpj.2013.03.047CrossRefGoogle ScholarPubMed
Coles, J.A. & Schneider-Picard, G. (1989). Amplification of small signals by voltage-gated sodium channels in drone photoreceptors. Journal of Comparative Physiology A 165, 109–118.10.1007/BF00613804CrossRefGoogle ScholarPubMed
Collett, T.S. & Land, M.F. (1975). Visual control of flight behaviour in the Hoverflysyritta Pipiens L. Journal of Comparative Physiology A 99, 1–66.10.1007/BF01464710CrossRefGoogle Scholar
Fain, G.L. & Lisman, J.E. (1981). Membrane conductances of photoreceptors. Progress in Biophysics and Molecular Biology 37, 91–147.CrossRefGoogle ScholarPubMed
Fischer, S., Meyer-Rochow, V.B. & Muller, C.H. (2012). Challenging limits: Ultrastructure and size-related functional constraints of the compound eye of Stigmella Microtheriella (Lepidoptera: Nepticulidae). Journal of Morphology 273, 1064–1078.CrossRefGoogle Scholar
Fischer, S., Muller, C.H. & Meyer-Rochow, V.B. (2011). How small can small be: The compound eye of the Parasitoid wasp Trichogramma Evanescens (Westwood, 1833) (hymenoptera, Hexapoda), an insect of 0.3- to 0.4-mm total body size. Visual Neuroscience 28, 295–308.CrossRefGoogle Scholar
Franceschini, N., Hardie, R., Ribi, W. & Kirschfeld, K. (1981). Sexual dimorphism in a photoreceptor. Nature 291, 241–244.CrossRefGoogle Scholar
Frolov, R.V. & Ignatova, I.I. (2020a). Speed of phototransduction in the microvillus regulates the accuracy and bandwidth of the rhabdomeric photoreceptor. PLoS Computational Biology 16, e1008427.10.1371/journal.pcbi.1008427CrossRefGoogle Scholar
Frolov, R.V. & Ignatova, I.I. (2020b). Electrophysiological adaptations of insect photoreceptors and their elementary responses to diurnal and nocturnal lifestyles. Journal of Comparative Physiology A 206, 55–69.10.1007/s00359-019-01392-8CrossRefGoogle Scholar
Fuortes, M.G. & Poggio, G.F. (1963). Transient responses to sudden illumination in cells of the eye of limulus. The Journal of General Physiology 46, 435–452.CrossRefGoogle ScholarPubMed
Gonzalez-Bellido, P.T., Wardill, T.J. & Juusola, M. (2011). Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands. Proceedings of the National Academy of Sciences of the United States of America 108, 4224–4229.10.1073/pnas.1014438108CrossRefGoogle ScholarPubMed
Gu, Y., Oberwinkler, J., Postma, M. & Hardie, R.C. (2005). Mechanisms of light adaptation in drosophila photoreceptors. Current Biology: CB 15, 1228–1234.CrossRefGoogle ScholarPubMed
Hardie, R.C. (2012). Phototransduction mechanisms in drosophila microvillar photoreceptors. Wiley Interdisciplinary Reviews: Membrane Transport and Signaling 1, 162–187.Google Scholar
Hardie, R.C., Franceschini, N., Ribi, W. & Kirschfeld, K. (1981). Distribution and properties of sex-specific photoreceptors in the Fly Musca domestica. Journal of Comparative Physiology A 145, 139–152.CrossRefGoogle Scholar
Hardie, R.C. & Juusola, M. (2015). Phototransduction in drosophila. Current Opinion in Neurobiology 34, 37–45.CrossRefGoogle ScholarPubMed
Heras, F.J., Laughlin, S.B. & Niven, J.E. (2016). Shunt peaking in neural membranes. Journal of the Royal Society, Interface 13, 20160719.CrossRefGoogle ScholarPubMed
Hornstein, E.P., O’Carroll, D.C., Anderson, J.C. & Laughlin, S.B. (2000). Sexual dimorphism matches photoreceptor performance to behavioural requirements. Proceedings Biological Sciences 267, 2111–2117.CrossRefGoogle ScholarPubMed
Horridge, G.A. (1978). The separation of visual axes in apposition compound eyes. Philosophical Transactions of the Royal Society of London Series B, Biological sciences 285, 1–59.Google ScholarPubMed
Horridge, G.A. & Duelli, P. (1979). Anatomy of the regional differences in the eye of the mantis ciulfina. Journal of Experimental Biology 80, 165–190.CrossRefGoogle Scholar
Horridge, G.A., Mimura, K. & Hardie, R.C. (1976). Fly photoreceptors. III. Angular sensitivity as a function of wavelength and the limits of resolution. Proceedings of the Royal Society of London Series B Biological Sciences 194, 151–177.Google Scholar
Howard, J., Dubs, A. & Payne, R. (1984). The dynamics of phototransduction in insects. Journal of Comparative Physiology A 154, 707–718.CrossRefGoogle Scholar
Ignatova, I.I., French, A.S. & Frolov, R.V. (2018). Effects of phase correlations in naturalistic stimuli on quantitative information coding by fly photoreceptors. Journal of Neurophysiology 119, 2276–2290.CrossRefGoogle ScholarPubMed
Juusola, M. & Hardie, R.C. (2001). Light adaptation in drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25°C. The Journal of General Physiology 117, 3–25.CrossRefGoogle ScholarPubMed
Katz, B., Voolstra, O., Tzadok, H., Yasin, B., Rhodes-Modrov, E., Bartels, J.P., Strauch, L., Huber, A. & Minke, B. (2017). The latency of the light response is modulated by the phosphorylation state of drosophila Trp at a specific site. Channels 11, 678–685.CrossRefGoogle ScholarPubMed
Kirschfeld, K. (1976). The resolution of lens and compound eyes. In Neural Principles in Vision, ed. Zettler, F. & Weiler, R., pp. 354–370. Berlin: Springer.CrossRefGoogle Scholar
Kirschfeld, K. & Wenk, P. (1976). The dorsal compound eye of simuliid flies: An eye specialized for the detection of small, rapidly moving objects. Zeitschrift fur Naturforschung Section C, Biosciences 31, 764–765.CrossRefGoogle ScholarPubMed
Labhart, T. & Nilsson, D.E. (1995). The dorsal eye of the dragonfly sympetrum: Specializations for prey detection against the blue sky. Journal of Comparative Physiology A 176, 437–453.10.1007/BF00196410CrossRefGoogle Scholar
Land, M.F. (1997). Visual acuity in insects. Annual Review of Entomology 42, 147–177.CrossRefGoogle ScholarPubMed
Land, M.F. & Eckert, H. (1985). Maps of the acute zones of fly eyes. Journal of Comparative Physiology A 156, 525–538.CrossRefGoogle Scholar
Laughlin, S.B. (1994). Matching coding, circuits, cells, and molecules to signals: General principles of retinal design in the fly’s eye. Progress in Retinal and Eye Research 13, 165–196.CrossRefGoogle Scholar
Laughlin, S.B. & Weckström, M. (1993). Fast and slow photoreceptors – A comparative study of the functional diversity of coding and conductances in the diptera. Journal of Comparative Physiology A 172, 593–609.10.1007/BF00213682CrossRefGoogle Scholar
Menzel, J.G., Wunderer, H. & Stavenga, D.G. (1991). Functional morphology of the divided compound eye of the honeybee drone (Apis Mellifera). Tissue & Cell 23, 525–535.CrossRefGoogle Scholar
Nikolic, K., Loizu, J., Degenaar, P. & Toumazou, C. (2010). A stochastic model of the single photon response in drosophila photoreceptors. Integrative Biology 2, 354–370.CrossRefGoogle ScholarPubMed
O’Grady, G.E. & Mciver, S.B. (1987). Fine structure of the compound eye of the black Fly Simulium Vittatum (Diptera: Simuliidae). Canadian Journal of Zoology 65, 1454–1469.CrossRefGoogle Scholar
Pask, C. & Barrell, K.F. (1980). Photoreceptor optics II: Application to angular sensitivity and other properties of a lens-photoreceptor system. Biological Cybernetics 36, 9–18.CrossRefGoogle ScholarPubMed
Rossel, S. (1979). Regional differences in photoreceptor performance in the eye of the praying mantis. Journal of Comparative Physiology A 131, 95–112.CrossRefGoogle Scholar
Snyder, A.W. (1975). Photoreceptor optics - theoretical principles. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Snyder, A.W. (1977). Acuity of compound eyes: Physical limitations and design. Journal of Comparative Physiology A 116, 161–182.CrossRefGoogle Scholar
Snyder, A.W. & Miller, W.H. (1972). Fly colour vision. Vision Research 12, 1389–IN1382.CrossRefGoogle ScholarPubMed
Stavenga, D.G. (2004a). Angular and spectral sensitivity of Fly photoreceptors. III. Dependence on the pupil mechanism in the blowfly Calliphora. Journal of Comparative Physiology A 190, 115–129.CrossRefGoogle Scholar
Stavenga, D.G. (2004b). Visual acuity of Fly photoreceptors in natural conditions – Dependence on UV sensitizing pigment and light-controlling pupil. Journal of Experimental Biology 207, 1703–1713.CrossRefGoogle Scholar
Tatler, B., O’Carroll, D.C. & Laughlin, S.B. (2000). Temperature and the temporal resolving power of Fly photoreceptors. Journal of Comparative Physiology A 186, 399–407.CrossRefGoogle ScholarPubMed
Vallet, A.M., Coles, J.A., Eilbeck, J.C. & Scott, A.C. (1992). Membrane conductances involved in amplification of small signals by sodium channels in photoreceptors of drone honey bee. The Journal of Physiology 456, 303–324.CrossRefGoogle ScholarPubMed
Van Hateren, J. (1984). Waveguide theory applied to optically measured angular sensitivities of fly photoreceptors. Journal of Comparative Physiology A 154, 761–771.CrossRefGoogle Scholar
Van Hateren, J. (1997). Processing of natural time series of intensities by the visual system of the blowfly. Vision Research 37, 3407–3416.CrossRefGoogle ScholarPubMed
Van Hateren, J., Hardie, R.C., Rudolph, A., Laughlin, S.B. & Stavenga, D.G. (1989). The bright zone, a specialized dorsal eye region in the male Blowflychrysomyia Megacephala. Journal of Comparative Physiology A 164, 297–308.CrossRefGoogle Scholar
Van Hateren, J. & Snippe, H.P. (2001). Information theoretical evaluation of parametric models of gain control in blowfly photoreceptor cells. Vision Research 41, 1851–1865.CrossRefGoogle ScholarPubMed
Voolstra, O., Beck, K., Oberegelsbacher, C., Pfannstiel, J. & Huber, A. (2010). Light-dependent phosphorylation of the drosophila transient receptor potential ion channel. The Journal of Biological Chemistry 285, 14275–14284.CrossRefGoogle ScholarPubMed
Wardill, T.J., Fabian, S.T., Pettigrew, A.C., Stavenga, D.G., Nordstrom, K. & Gonzalez-Bellido, P.T. (2017). A novel interception strategy in a miniature robber Fly with extreme visual acuity. Current biology: CB 27, 854–859.CrossRefGoogle Scholar
Warrant, E.J. (2016). Sensory matched filters. Current Biology: CB 26, R976–R980.CrossRefGoogle ScholarPubMed
Weckstrom, M., Hardie, R.C. & Laughlin, S.B. (1991). Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation. The Journal of Physiology 440, 635–657.CrossRefGoogle ScholarPubMed
Weckström, M., Jarvilehto, M. & Heimonen, K. (1993). Spike-like potentials in the axons of nonspiking photoreceptors. Journal of Neurophysiology 69, 293–296.CrossRefGoogle ScholarPubMed
Weckström, M., Juusola, M. & Laughlin, S.B. (1992). Presynaptic enhancement of signal transients in photoreceptor terminals in the compound eye. Proceedings of the Royal Society of London Series B: Biological Sciences 250, 83–89.Google Scholar
Zeil, J. (1983). Sexual dimorphism in the visual system of flies: The compound eyes and neural superposition in Bibionidae (Diptera). Journal of Comparative Physiology A 150, 379–393.CrossRefGoogle Scholar