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The sources of electrophysiological variability in the retina of Periplaneta americana

Published online by Cambridge University Press:  12 March 2019

Roman V. Frolov Open the ORCID record for Roman V. Frolov [Opens in a new window]
Roman V. Frolov*
Affiliation:
Nano and Molecular Systems Research Unit, Faculty of Science, University of Oulu, Oulun Yliopisto 90014, Finland
*
*Address correspondence: Roman V. Frolov, Email: [email protected]
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Abstract

Variability in the electrophysiological properties of homotypic photoreceptors is widespread and is thought to facilitate functioning under disparate illumination conditions. Compound eyes of insects have three sources of variability: inter-individual, intra-individual, and intra-ommatidial, the latter two overlapping. Here, I explored the causes of variability in Periplaneta americana, a nocturnal insect characterized by highly variable photoreceptor responses. By recording from photoreceptors in dissociated ommatidia, including consecutive recordings from photoreceptors in the same ommatidium (SO), I studied the variability of six properties: whole-cell membrane capacitance (Cm), phototransduction latency, maximal conductance (Gmax) and the slope factor of the sustained Kv current, absolute sensitivity in dim light, and sustained light-induced current (LIC) amplitude in bright light. Coefficient of variation (CV) metrics were used to compare variances in four experimental groups: SO, same animal (SA), all data combined “full sample” (FS), and full sample of all SO recordings (FSSO). For the normally distributed parameters Cm, Gmax, slope factor, and latency, the highest CV values were found in FS and FSSO, intermediate in SA, and the lowest in SO. On average, SO variance accounted for 47% of the full-sample variance in these four parameters. Absolute sensitivity and LIC values were not normally distributed, and the differences in variability between SO and FS/FSSO groups were smaller than for the other four parameters. These results indicate two main sources of variability, intra-ommatidial and inter-individual. Inter-individual variability was investigated by exposing adult cockroaches to constant light or dark for several months. In both groups, the majority of CV measures for the six parameters decreased compared to control, indicating substantial contribution of phenotypic plasticity to inter-individual differences. Analysis of variability of resting potential and elementary voltage responses revealed that resting potential is mainly determined by the sustained Kv conductance, whereas voltage bump amplitude is mainly determined by current bump amplitude and Cm.

Keywords

PhotoreceptorMembrane capacitancePhysiological variabilityPotassium currentphotoreceptor latency
Type
Research Article
Information
Visual Neuroscience , Volume 36 , 2019 , E003
Copyright
Copyright © Cambridge University Press 2019 

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References

Arikawa, K. & Uchiyama, H. (1996). Red receptors dominate the proximal tier of the retina in the butterfly Papilio xuthus. Journal of Comparative Physiology 178, 55–61.Google Scholar
Bolch, B.W. (1968). More on unbiased estimation of the standard deviation. The American Statistician 22, 27.Google Scholar
Chyb, S., Hevers, W., Forte, M., Wolfgang, W.J., Selinger, Z. & Hardie, R.C. (1999). Modulation of the light response by cAMP in Drosophila photoreceptors. Journal of Neuroscience 19, 8799–8807.CrossRefGoogle ScholarPubMed
Curcio, C.A., Sloan, K.R. Jr., Packer, O., Hendrickson, A.E. & Kalina, R.E. (1987). Distribution of cones in human and monkey retina: Individual variability and radial asymmetry. Science 236, 579–582.CrossRefGoogle ScholarPubMed
Frolov, R., Immonen, E.V., Vahasoyrinki, M. & Weckstrom, M. (2012). Postembryonic developmental changes in photoreceptors of the stick insect Carausius morosus enhance the shift to an adult nocturnal life-style. Journal of Neuroscience 32, 16821–16831.CrossRefGoogle Scholar
Frolov, R. & Weckstrom, M. (2014). Developmental changes in biophysical properties of photoreceptors in the common water strider (Gerris lacustris): Better performance at higher cost. Journal of Neurophysiology 112, 913–922.CrossRefGoogle ScholarPubMed
Frolov, R.V. (2015). Biophysical properties of photoreceptors in Corixa punctata facilitate diurnal life-style. Vision Research 111, 75–81.CrossRefGoogle ScholarPubMed
Frolov, R.V. (2016). Current advances in invertebrate vision: Insights from patch-clamp studies of photoreceptors in apposition eyes. Journal of Neurophysiology 116, 709–723.CrossRefGoogle ScholarPubMed
Frolov, R.V., Immonen, E.V., Saari, P., Torkkeli, P.H., Liu, H. & French, A.S. (2018). Phenotypic plasticity in Periplaneta americana photoreceptors. The Journal of General Physiology 150, 1386–1396.Google ScholarPubMed
Frolov, R.V., Immonen, E.V. & Weckstrom, M. (2014). Performance of blue- and green-sensitive photoreceptors of the cricket Gryllus bimaculatus. Journal of Comparative Physiology 200, 209–219.CrossRefGoogle ScholarPubMed
Frolov, R.V., Matsushita, A. & Arikawa, K. (2017). Not flying blind: A comparative study of photoreceptor function in flying and non-flying cockroaches. Journal of Experimental Biology 220, 2335–2344.CrossRefGoogle ScholarPubMed
Heimonen, K., Immonen, E.V., Frolov, R.V., Salmela, I., Juusola, M., Vahasoyrinki, M. & Weckstrom, M. (2012). Signal coding in cockroach photoreceptors is tuned to dim environments. Journal of Neurophysiology 108, 2641–2652.CrossRefGoogle ScholarPubMed
Heimonen, K., Salmela, I., Kontiokari, P. & Weckstrom, M. (2006). Large functional variability in cockroach photoreceptors: Optimization to low light levels. Journal of Neuroscience 26, 13454–13462.CrossRefGoogle ScholarPubMed
Hendrickson, A. (2005). Organization of the adult primate fovea. In Macular Degeneration, eds., Penfold, P.L. & Provis, J.M., pp. 1–23. Berlin, Heidelberg: Springer Berlin Heidelberg.Google Scholar
Immonen, E.V., French, A.S., Torkkeli, P.H., Liu, H., Vahasoyrinki, M. & Frolov, R.V. (2017). EAG channels expressed in microvillar photoreceptors are unsuited to diurnal vision. The Journal of Physiology 595, 5465–5479.CrossRefGoogle ScholarPubMed
Immonen, E.V., Ignatova, I., Gislen, A., Warrant, E., Vahasoyrinki, M., Weckstrom, M. & Frolov, R. (2014a). Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer. Proceedings of the Royal Society of London, Series B: Biological Sciences 281.CrossRefGoogle Scholar
Immonen, E.V., Krause, S., Krause, Y., Frolov, R., Vahasoyrinki, M.T. & Weckstrom, M. (2014b). Elementary and macroscopic light-induced currents and their Ca2+-dependence in the photoreceptors of Periplaneta americana. Frontiers in Physiology 5, 153.CrossRefGoogle Scholar
Islas, L.D. & Sigworth, F.J. (1999). Voltage sensitivity and gating charge in Shaker and Shab family potassium channels. The Journal of General Physiology 114, 723–742.CrossRefGoogle ScholarPubMed
Kelly, K.M. & Mote, M.I. (1990). Avoidance of monochromatic light by the cockroach Periplaneta americana. Journal of Insect Physiology 36, 287–291.CrossRefGoogle Scholar
Ryan, M.Y., Maloney, R., Fineberg, J.D., Reenan, R.A. & Horn, R. (2012). RNA editing in eag potassium channels: Biophysical consequences of editing a conserved S6 residue. Channels 6, 443–452.CrossRefGoogle ScholarPubMed
Saari, P., French, A.S., Torkkeli, P.H., Liu, H., Immonen, E.V. & Frolov, R.V. (2017). Distinct roles of light-activated channels TRP and TRPL in photoreceptors of Periplaneta americana. The Journal of General Physiology 149, 455–464.CrossRefGoogle ScholarPubMed
Salmela, I., Immonen, E.V., Frolov, R., Krause, S., Krause, Y., Vahasoyrinki, M. & Weckstrom, M. (2012). Cellular elements for seeing in the dark: Voltage-dependent conductances in cockroach photoreceptors. BMC Neuroscience 13, 93.CrossRefGoogle ScholarPubMed
Scott, K. & Zuker, C.S. (1998). Assembly of the Drosophila phototransduction cascade into a signalling complex shapes elementary responses. Nature 395, 805.CrossRefGoogle ScholarPubMed
Snyder, A.W., Menzel, R. & Laughlin, S.B. (1973). Structure and function of the fused rhabdom. Journal of Comparative Physiology 87, 99–135.CrossRefGoogle Scholar
Wolfram, V. & Juusola, M. (2004). Impact of rearing conditions and short-term light exposure on signaling performance in Drosophila photoreceptors. Journal of Neurophysiology 92, 1918–1927.CrossRefGoogle ScholarPubMed
Zhou, S., Flamier, A., Abdouh, M., Tétreault, N., Barabino, A., Wadhwa, S. & Bernier, G. (2015). Differentiation of human embryonic stem cells into cone photoreceptors through simultaneous inhibition of BMP, TGFβ and Wnt signaling. Development 142, 3294–3306.CrossRefGoogle ScholarPubMed