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Performance of blue- and green-sensitive photoreceptors of the cricket Gryllus bimaculatus

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Abstract

The compound eye of the cricket Gryllus bimaculatus contains a specialized dorsal rim area (DRA) populated by distinct blue-sensitive photoreceptors responsible for perception of polarized light. The rest of the eye is dominated by green-sensitive photoreceptors. Using patch clamp we studied dissociated ommatidia of nocturnal adults and diurnal eight-instar nymphs with the goals (1) of characterizing the biophysical properties of cricket photoreceptors in general and (2) describing the functionally dissimilar blue- and green-sensitive photoreceptors in terms of voltage-gated channel composition and signal coding. Despite different lifestyles, adult and nymph photoreceptors were indistinguishable. No significant circadian changes were observed in K+ currents. In contrast, prominent differences were seen between blue- and green-sensitive photoreceptors. The former were characterized by relatively low absolute sensitivity, high input resistance, slow quantum bumps with long latencies, small light-induced and K+ currents and low steady-state depolarization. Information rate, a measure of photoreceptor performance calculated from voltage responses to bandwidth-limited white noise-modulated light contrast, was 87 ± 8 bits s−1 in green-sensitive photoreceptors vs. 59 ± 14 bits s−1 in blue-sensitive photoreceptors, implying a limited role of DRA in the perception of visual contrasts. In addition, evidence of electrical coupling between photoreceptors is presented.

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References

  • Abe Y, Ushirogawa H, Tomioka K (1997) Circadian locomotor rhythms in the cricket, Gryllodes sigillatus. I. Localization of the pacemaker and the photoreceptor. Zool Sci 14:719–727

    Article  CAS  PubMed  Google Scholar 

  • Blum M, Labhart T (2000) Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye. J Comp Physiol A 186:119–128

    Article  CAS  PubMed  Google Scholar 

  • Cuttle MF, Hevers W, Laughlin SB, Hardie RC (1995) Diurnal modulation of photoreceptor potassium conductance in the locust. J Comp Physiol 176:307–316

    Article  CAS  Google Scholar 

  • Danbara Y, Sakamoto T, Uryu O, Tomioka K (2010) RNA interference of timeless gene does not disrupt circadian locomotor rhythms in the cricket Gryllus bimaculatus. J Insect Physiol 56:1738–1745

    Article  CAS  PubMed  Google Scholar 

  • Dyakonova VE, Krushinsky AL (2013) Serotonin precursor (5-hydroxytryptophan) causes substantial changes in the fighting behavior of male crickets, Gryllus bimaculatus. J Comp Physiol A 99:601–609

    Article  Google Scholar 

  • Faivre O, Juusola M (2008) Visual coding in locust photoreceptors. PLoS One 3:e2173

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 32:16821–16831

    Article  CAS  PubMed  Google Scholar 

  • Grobe B, Rothbart MM, Hanschke A, Hennig RM (2012) Auditory processing at two time scales by the cricket Gryllus bimaculatus. J Exp Biol 215:1681–1690

    Article  PubMed  Google Scholar 

  • Harrison SJ, Thomson IR, Grant CM, Bertram SM (2013) Calling, courtship, and condition in the fall field cricket, Gryllus pennsylvanicus. PLoS One 8:e60356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heisenberg M, Buchner E (1977) The rôle of retinula cell types in visual behavior of Drosophila melanogaster. J Comp Physiol 117:127–162

    Article  Google Scholar 

  • Henderson SR, Reuss H, Hardie RC (2000) Single photon responses in Drosophila photoreceptors and their regulation by Ca2+. J Physiol 524(Pt 1):179–194

    Article  CAS  PubMed  Google Scholar 

  • Henze MJ, Dannenhauer K, Kohler M, Labhart T, Gesemann M (2012) Opsin evolution and expression in arthropod compound eyes and ocelli: insights from the cricket Gryllus bimaculatus. BMC Evol Biol 12:163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hirtenlehner S, Kung S, Kainz F, Romer H (2013) Asymmetry in the song of crickets: preferences of females and proximate mechanism of discrimination. J Exp Biol 216:2046–2054

    Article  PubMed  Google Scholar 

  • Itoh MT, Hattori A, Sumi Y, Suzuki T (1995) Day–night changes in melatonin levels in different organs of the cricket (Gryllus bimaculatus). J Pineal Res 18:165–169

    Article  CAS  PubMed  Google Scholar 

  • Kainz F, Ewen-Campen B, Akam M, Extavour CG (2011) Notch/Delta signalling is not required for segment generation in the basally branching insect Gryllus bimaculatus. Development 138:5015–5026

    Article  CAS  PubMed  Google Scholar 

  • Kouvalainen E, Weckström M, Juusola M (1994) A method for determining photoreceptor signal-to-noise ratio in the time and frequency domains with a pseudorandom stimulus. Vis Neurosci 11:1221–1225

    Article  CAS  PubMed  Google Scholar 

  • Krause Y, Krause S, Huang J, Liu CH, Hardie RC, Weckström M (2008) Light-dependent modulation of Shab channels via phosphoinositide depletion in Drosophila photoreceptors. Neuron 59:596–607

    Article  CAS  PubMed  Google Scholar 

  • Labhart T (1988) Polarization-opponent interneurons in the insect visual system. Nature 331:435–437

    Article  Google Scholar 

  • Labhart T (1999) How polarization-sensitive interneurons of crickets see the polarization pattern of the sky: a field study with an opto-electronic model neurone. J Exp Biol 202:757–770

    PubMed  Google Scholar 

  • Labhart T, Keller K (1992) Fine structure and growth of the polarization-sensitive dorsal rim area in the compound eye of larval crickets. Naturwissenschaften 79:527–529

    Article  Google Scholar 

  • Labhart T, Hodel B, Valenzuela I (1984) The physiology of the cricket’s compound eye with particular reference to the anatomically specialized dorsal rim area. J Comp Physiol 155:289–296

    Article  Google Scholar 

  • Laughlin SB (1996) Matched filtering by a photoreceptor membrane. Vis Res 36:1529–1541

    Article  CAS  PubMed  Google Scholar 

  • Laughlin SB, Weckström M (1993) Fast and slow photoreceptors—a comparative study of the functional diversity of coding and conductances in the Diptera. J Comp Physiol 172:593–609

    Article  Google Scholar 

  • Laughlin SB, de Ruyter van Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41

    Article  CAS  PubMed  Google Scholar 

  • Lillywhite PG (1978) Coupling between locust photoreceptors revealed by a study of quantum bumps. J Comp Physiol 125:13–27

    Article  Google Scholar 

  • Niven JE, Vähäsöyrinki M, Juusola M (2003a) Shaker K(+)-channels are predicted to reduce the metabolic cost of neural information in Drosophila photoreceptors. Proc Biol Sci 270(Suppl 1):S58–S61

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Niven JE, Vähäsöyrinki M, Kauranen M, Hardie RC, Juusola M, Weckström M (2003b) The contribution of Shaker K+ channels to the information capacity of Drosophila photoreceptors. Nature 421:630–634

    Article  CAS  PubMed  Google Scholar 

  • Niven JE, Anderson JC, Laughlin SB (2007) Fly photoreceptors demonstrate energy-information trade-offs in neural coding. PLoS Biol 5:e116

    Article  PubMed Central  PubMed  Google Scholar 

  • Ribelayga C, Cao Y, Mangel SC (2008) The circadian clock in the retina controls rod–cone coupling. Neuron 59:790–801

    Article  CAS  PubMed  Google Scholar 

  • Sakura M, Aonuma H (2013) Aggressive behavior in the antennectomized male cricket Gryllus bimaculatus. J Exp Biol 216:2221–2228

    Article  PubMed  Google Scholar 

  • Sakura M, Takasuga K, Watanabe M, Eguchi E (2003) Diurnal and circadian rhythm in compound eye of cricket (Gryllus bimaculatus): changes in structure and photon capture efficiency. Zool Sci 20:833–840

    Article  PubMed  Google Scholar 

  • Salmela I, Immonen EV, Frolov R, Krause S, Krause Y, Vähäsöyrinki M, Weckström M (2012) Cellular elements for seeing in the dark: voltage-dependent conductances in cockroach photoreceptors. BMC Neurosci 13:93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smakman JGJ, Stavenga DG (1987) Angular sensitivity of blowfly photoreceptors: broadening by artificial electrical coupling. J Comp Physiol 160:501–507

    Article  Google Scholar 

  • 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 22:1371–1380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tessier-Lavigne M, Attwell D (1988) The effect of photoreceptor coupling and synapse nonlinearity on signal:noise ratio in early visual processing. Proc R Soc Lond B Biol Sci 234:171–197

    Article  CAS  PubMed  Google Scholar 

  • Tomioka K (2000) Protein synthesis is a required process for the optic lobe circadian clock in the cricket Gryllus bimaculatus. J Insect Physiol 46:281–287

    Article  CAS  PubMed  Google Scholar 

  • Tomioka K, Chiba Y (1982) Post-embryonic development of circadian rhythm in the cricket, Gryllus bimaculatus: a rhythm reversal. J Comp Physiol 147:299–304

    Article  Google Scholar 

  • Uryu O, Kamae Y, Tomioka K, Yoshii T (2013) Long-term effect of systemic RNA interference on circadian clock genes in hemimetabolous insects. J Insect Physiol 59:494–499

    Article  CAS  PubMed  Google Scholar 

  • Vähäkainu A, Vähäsöyrinki M, Weckström M (2013) Membrane filtering properties of the bumblebee (Bombus terrestris) photoreceptors across three spectral classes. J Comp Physiol A 199:629–639

    Article  Google Scholar 

  • Vähäsöyrinki M, Niven JE, Hardie RC, Weckström M, Juusola M (2006) Robustness of neural coding in Drosophila photoreceptors in the absence of slow delayed rectifier K+ channels. J Neurosci 26:2652–2660

    Article  PubMed  Google Scholar 

  • van Hateren JH, van der Schaaf A (1998) Independent component filters of natural images compared with simple cells in primary visual cortex. Proc Biol Sci 265:359–366

    Article  PubMed Central  PubMed  Google Scholar 

  • Warrant E, Nilsson D-E (eds) (2006) Invertebrate vision. Cambridge University Press, Cambridge

    Google Scholar 

  • Weckström M, Laughlin SB (1995) Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends Neurosci 18:17–21

    Article  PubMed  Google Scholar 

  • Weckström M, Hardie RC, Laughlin SB (1991) Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation. J Physiol 440:635–657

    PubMed  Google Scholar 

  • Yamaguchi S, Wolf R, Desplan C, Heisenberg M (2008) Motion vision is independent of color in Drosophila. Proc Natl Acad Sci 105:4910–4915

    Article  CAS  PubMed  Google Scholar 

  • Zufall F, Schmitt M, Menzel R (1989) Spectral and polarized light sensitivity of photoreceptors in the compound eye of the cricket (Gryllus bimaculatus). J Comp Physiol A 164:597–608

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the Academy of Finland to R. F and M. W. and from the Finnish Graduate School of Neuroscience and the Finnish Cultural Foundation to E-V. I. The authors declare no conflict of interest.

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Authors and Affiliations

  1. Division of Biophysics, Department of Physics, University of Oulu, PO BOX 3000, 90014, Oulu, Finland

    Roman V. Frolov, Esa-Ville Immonen & Matti Weckström

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  1. Roman V. Frolov
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  2. Esa-Ville Immonen
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  3. Matti Weckström
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Correspondence to Roman V. Frolov.

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R.V. Frolov and E.-V. Immonen contributed equally to the study.

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Frolov, R.V., Immonen, EV. & Weckström, M. Performance of blue- and green-sensitive photoreceptors of the cricket Gryllus bimaculatus . J Comp Physiol A 200, 209–219 (2014). https://doi.org/10.1007/s00359-013-0879-6

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