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Insect Optomotor Experiments in the Dark Using Virtual Reality University of Oulu Graduate School, P.O

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Insect Optomotor Experiments in the Dark Using Virtual Reality University of Oulu Graduate School, P.O INSECT OPTOMOTOR EXPERIMENTS IN THE DARK USING VIRTUAL REALITY ANNA HONKANEN REPORT SERIES IN PHYSICAL SCIENCES Report No. 94 (2014) INSECT OPTOMOTOR EXPERIMENTS IN THE DARK USING VIRTUAL REALITY ANNA HONKANEN Department of Physics University of Oulu Finland Academic dissertation to be presented, with the permission of the Doctoral Training Committee for Technology and Natural Science of the University of Oulu, for public discussion in the Auditorium YB210, Linnanmaa, on 15th December, 2014, at 12 o’clock noon. REPORT SERIES IN PHYSICAL SCIENCES Report No. 94 OULU 2014 ŏ UNIVERSITY OF OULU Opponent Professor David O’Carroll, Lund University, Sweden Reviewers Associate Professor Marie Dacke, Lund University, Sweden Dr. Rafael Kurtz, Bielefeld University, Germany Custos Professor Matti Weckström, University of Oulu, Finland ISBN 978-952-62-0701-8 ISBN 978-952-62-0702-5 (PDF) ISSN 1239-4327 Juvenes Print Oulu 2014 Sinun pitää aloittaa se väikkäri sanoin: “Jo muinaiset foinikialaiset…” -V.T. Honkanen, Anna: Insect optomotor experiments in the dark using virtual reality University of Oulu Graduate School, P.O. Box 8100, FI-90014, University of Oulu, Finland; Faculty of Science, Department of Physics, Division of Biophysics, University of Oulu, P.O. Box 3000, FI-90014, University of Oulu, Finland; Biocenter Oulu, P.O. Box 5000, FI-90014, University of Oulu, Finland Report Series in Physical Sciences No. 94 (2014) Abstract Vision is capable of providing an animal with a wealth of information very fast. Visually guided behaviours are numerous, ranging from foraging to navigation. Vision can be quite reliable in bright light, but the signals produced by the photoreceptors become progressively more unreliable with falling light intensities. In this thesis the usefulness of a novel virtual reality-based environment for insect vision research is reviewed, and the low-light vision of the American cockroach, Periplaneta americana, is assessed using the optomotor behavioural paradigm and intracellular photoreceptor recordings. The optomotor reaction is visual behaviour where an animal responds to a rotation of its environment by following the movement of its surroundings with its eyes or - like insects - by rotating its body in the direction of the movement. Placing the cockroach on a trackball in the middle of the virtual reality apparatus and projecting a rotating pattern of vertical stripes around it invariably causes an optomotor reaction if the cockroach is able to see the moving pattern. Presenting the cockroaches with the stimulus pattern at different low light levels and observing their abilities to follow the movement reveal the lowest light intensity at which they are able to use vision in guiding their behaviour. The compound eye photoreceptor signals at this behavioural threshold consist of single- photon absorption events called ‘bumps’ at the extremely low rate of one bump every ten seconds. Furthermore, the role of the simple eyes or ocelli in the low-light vision of the cockroach is studied in the virtual reality by covering the compound eyes, the ocelli, or both. The ocelli seem to measure the light intensity and communicate this information to the compound eyes, and also have a direct effect on the general activity level of the cockroach. Keywords: virtual reality, optomotor reaction, behaviour, intracellular, photoreceptor, compound eyes, ocelli Acknowledgements This thesis was written and the research presented in it conducted at the Division of Biophysics of the Department of Physics at the University of Oulu, and Biocenter Oulu. The research was funded by Biocenter Oulu and the writing process by the University of Oulu Graduate School. I want to thank my primary supervisor Kyösti Heimonen for guiding a biologist into the world of biophysics. Thanks for all the conversations, for teaching me the fine art of intracellular recordings, and for being very patient although I’m not always the fastest cockroach on the trackball. Thanks to my second supervisor Mikko Vähäsöyrinki for the follow-up meetings and the short and accurate answers to my meandering questions. A huge thank you to my third supervisor, Professor Matti Weckström, for being tremendously supportive during all the writing I’ve done in the last year and a half. Although you are the busiest man I know, you always find the time to make comments and improvements to my manuscripts and help me with paperwork and whatnot. It is greatly appreciated. I am also very grateful to the pre- examiners of this thesis, Associate Professor Marie Dacke and Dr. Rafael Kurtz, for the swift examination of and helpful comments on the manuscript. I owe thanks to all the co-authors of the publications included in this thesis, especially everyone involved in the designing and building the virtual reality set-up that made all this research possible. Thanks to everyone at the biophysics group for discussions (on- and off-topic), help, and friendship. Special thanks to Marru for the great working atmosphere in our room (although our pot plants don’t seem to think so); Jouni for help with anything involving computers or maths; and Esa and Mikko L. for fixing everything I broke. Thanks to the ‘big boys’ Arto, Tuomas, Iikka and Ekku for letting me tag along for lunch, coffee, and beer, and sorry that I’ve became such a bore lately. I also wish to thank the Lund Vision Group for my first glimpse into behavioural experiments in vision research when I was just starting my PhD process, and for giving me the opportunity to learn from them on many occasions since. You are a true inspiration. Friends have been an endless source of peer support during this process. Maria, my comrade-in-arms (-and-mischief), thanks for always being there. Nelli, thanks for being the Duracell Bunny that you are, always coming up with fun ideas to cheer everybody up! Thanks to Tuomo for being the loyal but blunt friend and to Janiika for all the tea and empathy. Thanks to fellow Tieteen Kananpojat Anni and Henni for sharing your struggles, and the Käpyjengi for all the good times. I also wish to thank my friends at Oulu Comics Society. Special thanks to Sinikka for a beautiful 7 friendship that has lasted for almost 20 years although we get to see each other way too rarely. For my physical and also mental well-being during the writing process I thank all the people and horses at Aaltokankaan ratsutallit. The time spent at ‘Aaltis’ were the only moments of my week when I managed to keep my thoughts off work. My family has always been extremely supportive, no matter how weird things I’ve ended up doing. Thanks to Pasi, Kaisa, Sampo and Saija for growing up with me, and your families for reminding me of what it was actually like. Thanks to Liisa for relaxing holidays and delicious dinners at Kuusjärvi. Heartfelt thanks to my parents Hilkka and Rauno for your unconditional love and for the trust you had in me from a very young age. Finally, thanks to my beloved Jyri for putting up with and taking care of me and Reiska, especially during these last few months. You cheered me up and spurred me forward when I was about to give up. Hopefully I can repay it all sooner or later. Thanks for being in my life. Oulu, November 24th 2014 Anna Honkanen 8 List of abbreviations c contrast CO2 carbon dioxide DA dark-adapted; dark adaptation DAG diacylglycerol EMD elementary movement detector FFF flicker fusion frequency Imax the highest luminance of the stimulus pattern Imin the lowest luminance of the stimulus pattern IP3 inositol 1,4,5-trisphosphate KCl Potassium chloride LA light-adapted; light adaptation LED light-emitting diode LIC light-induced current M 1) prefix mega (106), as in Mȍ 2) molar concentration, e.g. 2 M = 2 mol/l m 1) metre 2) prefix milli (10-3), as in mV N total number of animals used n 1) prefic nano (10-9), as in nm 2) number of measurements; number of cells recorded N.S. statistically non-significant PIP2 phosphatidylinositol 4,5-bisphosphate PLC phospholipase C SD standard deviation SNR signal-to-noise ratio TRP transient receptor potential channel TRPL TRP-like channel USB “universal serial bus” standard for data transfer UV ultra violet V volt, the unit of electrical potential difference Vm membrane voltage VR virtual reality ǻࢥ interommatidial angle Ȝ angular period of the stimulus, i.e. the width of one black-and-white repeat (°) 9 ȜȦ temporal frequency of the stimulus (Hz) IJ time constant (of motion detector integrator) ȍ ohm, the unit of electrical resistance Ȧ angular velocity of the stimulus (°/s) 10 List of original publications This thesis is based on the following publications, which are referred throughout the text by their Roman numerals: I Takalo J, Piironen A, Honkanen A, Lempeä M, Aikio M, Tuukkanen T & Vähäsöyrinki M (2012) A fast and flexible panoramic virtual reality system for behavioural and electrophysiological experiments. Sci Rep 2: 324. II Honkanen A, Takalo J, Heimonen K, Vähäsöyrinki M & Weckström M (2014) Cockroach optomotor responses below single photon level. J Exp Biol 217: 4262- 4268. III Honkanen A, Heimonen K & Weckström M (2014) The role of cockroach ocelli in optomotor performance. A manuscript. Contribution: I did all experiments in papers (II) and (III) and all behavioural experiments in (I). I was also responsible for their analyses. In addition, I was involved in planning all the papers and drafted the first version of papers (II) and (III). 11 12 Contents Abstract Acknowledgements 7 List of abbreviations 9 List of original publications 11 Contents 13 1 Introduction 15 2 Theoretical foundation 19 2.1 Insect vision and visual behaviour .......................................................... 19 2.2 The structure of insect compound eye ....................................................
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