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By Aylia Mohammadi a Thesis Submitted in Conformity with the Requirements for the Degree of Doctor of Philosophy Graduate Depart

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By Aylia Mohammadi a Thesis Submitted in Conformity with the Requirements for the Degree of Doctor of Philosophy Graduate Depart QUANTITATIVE BEHAVIORAL ANALYSIS OF THERMAL NOCICEPTION IN Caenorhabditis elegans: INVESTIGATION OF NEURAL SUBSTRATES SPATIALLY MEDIATING THE NOXIOUS RESPONSE, AND THE EFFECTS OF PHARMACOLOGICAL PERTURBATIONS. by Aylia Mohammadi A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Physics University of Toronto © Copyright 2013 by Aylia Mohammadi Abstract Quantitative behavioral analysis of thermal nociception in Caenorhabditis elegans: investigation of neural substrates spatially mediating the noxious response, and the effects of pharmacological perturbations. Aylia Mohammadi Doctor of Philosophy Graduate Department of Physics University of Toronto 2013 The nematode Caenorhabditis elegans possesses a relatively simple nervous system of only 302 neurons, but is able to perform an impressive range of complex behaviors. This dissertation aims to understand the neurobiology of behavior by quantifying, at the systems-level, the sen- sorimotor response to carefully controlled stimuli. Through neuronal or genetic perturbations to the system, we can begin to uncouple the behavior from the underlying circuitry. The be- havior studied here is thermal nociception, an escape response designed to protect an organism from potential tissue damage or harm from noxious heat. Vertebrates and invertebrates alike possess sensory neurons called nociceptors that detect noxious stimuli and relay the stimulus information to elicit an appropriate escape response. C. elegans is known to perform a reversal or forward response when presented with noxious stimuli at the head or tail, respectively. In this work, we develop a novel thermal stimulus assay with precise spatiotemporal control of an infrared pulse that targets small regions along the worm to spatially dissect the noxious re- sponse. We comprehensively quantify the nociceptive behavior, and identify key metrics that scale with intensity, such as speed in the escape state and the probability of certain behavioral states after the stimulus. Furthermore, we have mapped the behavioral receptive field of the worm along its body, and show a previously unreported probabilistic midbody behavior dis- tinct from the head and tail responses. Surprisingly, the worm is able to differentiate localized ii stimuli at the midbody that are as close as 80 microns. We identified PVD as the thermal no- ciceptor for the midbody response using calcium imaging, genetic ablation and laser ablation. This suggests PVD could be used as a model to study spatial discrimination at the level of a single nociceptor. This spatial specificity further extends to pharmacological perturbations of the system. In particular, the application of clinically used painkillers to the worm results in a knockdown of this nociceptive response, but does so in a spatially specific manner. These results are promising for future studies building upon the techniques developed here, as they evidentiate the use of C. elegans as a model organism to study pain. iii Acknowledgements First and foremost, I would like to thank my supervisor, William Ryu. Will’s breadth of knowledge and dedication to science truly inspires. Will gave me enough freedom to start this project from scratch and take it to new, unexpected, exciting places that really motivated and engaged me as a scientist. Not only did Will teach me a lot regarding the technical aspects of this work, but I also learned invaluable skills as an experimentalist in general. Will showed me the satisfaction that comes with a beautifully designed, simple experiment to test a hypothesis, and that if we let our curiosity guide us, we can learn new things when things don’t make sense at first. I would also like to thank the members of my committee, Asher Cutter and Anton Zilman, for their support during this process. I would also like to express my heartfelt gratitude to all the members of the Ryu lab: your friendship has made coming to the lab every day genuinely enjoyable. I know you all will continue to do great work, wherever life takes you. In particular, I would like to thank my co-authors, Jarlath Byrne Rodgers and Ippei Kotera, without whom this work would not have been possible. On a personal note, there are some very important people who have been instrumental in my accomplishing this goal. My in-laws, Vito and Christine Barbera, have been a second set of parents to me, offering me unconditional support, as only parents can, throughout the years. My sister-in-law, Lisa Barbera, has been a stellar example to me of a successful female scientist, and has given me much (solicited) advice to help with tough decisions. My sister, Shaista Raza, has been a silent but indispensable partner in everything I do. Words cannot begin to describe my appreciation of my two biggest cheerleaders, my parents Ali and Kulsoom Mohammadi, and how they have supported me my entire life, believing I am capable of achieving anything. This has been a long road, and they have been my pillars of strength every step of the way. My father was the first scientist I knew in life, and his passion for discovery has definitely rubbed off on me. iv Finally, none of this would be possible without the unconditional love and support of my husband, Paul Barbera. If there is anyone who rivals my parents for my biggest fan, it is Paul. He has supported me in every sense of the word from the very beginning, and I look forward to our future adventures. Our life together has brought me so much genuine and profound joy, it has made even the toughest situations bearable. Thank you, Paul, for everything. v Contents Abstract ii Acknowledgements iv Table of Contents viii List of Tables ix List of Figures x 1 General Introduction 1 1.1 Quantitative framework for studying thermal sensorimotor behavior . 2 1.2 Nociception and pain in mammals . 5 1.3 Noxious signal transduction . 7 1.4 Attempts to map the spatial sensitivity of nociception . 8 1.5 C. elegans as a model organism for the study of nociception and pain . 9 2 Thermal stimulus experiment and behavioral phenotyping 14 2.1 Introduction . 14 2.2 Instrumentation . 15 2.2.1 Worm Zapper V1 . 15 2.2.2 Worm Zapper V2 . 18 2.3 Characteristics of the noxious thermal pulse on a moving worm . 22 vi 2.4 High-content phenotyping . 25 3 Behavioral response of C. elegans to localized thermal stimuli 38 3.1 Abstract . 38 3.2 Background . 39 3.3 Results . 41 3.3.1 Novel assay for quantifying the noxious response and mapping the be- havioral receptive field . 41 3.3.2 Multi-parameter, high-content phenotyping of N2 noxious response for the head, midbody, and tail . 43 3.3.3 The noxious response is elicited by a temporal temperature gradient rather than a temperature threshold. 45 3.3.4 Spatial sensitivity of the midbody response . 47 3.3.5 Mutant behavioral analyses identify neurons involved in the midbody and tail responses . 47 3.3.6 PVD is required for the midbody and tail thermal noxious response . 51 3.3.7 PVD responds differently to spatially localized heat pulses targeted at different locations near the midbody . 53 3.3.8 Mutant strains show defective noxious behavior suggesting molecules involved in sensing heat at the midbody . 54 3.4 Discussion . 57 3.5 Conclusion . 60 3.6 Materials and Methods . 60 4 C. elegans as a model system for pain 65 4.1 Introduction . 65 4.1.1 Animal models in thermal pain research . 67 4.1.2 Opioid pharmacology . 69 vii 4.2 Evidence of a mu opioid receptor in C. elegans . 70 4.2.1 The thermal avoidance response is modulated by morphine and nalox- one at the midbody . 70 4.2.2 Preliminary mutant screen identifies MOR candidates in C. elegans . 73 4.3 C. elegans with defective receptor NMUR-2 display spatially sensitive im- paired nociception . 76 4.4 Materials and Methods . 79 4.5 Future directions . 79 4.6 Concluding remarks . 82 References 84 viii List of Tables 3.1 Mutant strains used for thermal nociception assay. 55 4.1 Results from BLASTP search identifying top matches between C. elegans re- ceptors and the human MOR . 74 ix List of Figures 1.1 Schematic of transmission of nociceptive signals from peripheral target tissue to the dorsal horn of the spinal cord. 6 1.2 Confocal image of the PVD neuron in C. elegans. 12 2.1 Worm Zapper V1 . 16 2.2 Temperature profile of an anesthetized worm on an agar plate. 17 2.3 Effect of the lid on the beam temperature at the surface of the agar . 18 2.4 Schematic of localized thermal stimulus assay. 19 2.5 Reducing beam size for Worm Zapper V2 with 100mm lens . 19 2.6 Sample pattern on receipt paper using IR laser . 20 2.7 Thermocouple measurements of 150mA 133ms pulse . 21 2.8 Thermal profile of 133 ms IR pulse measured using a thermal camera . 22 2.9 Spatial and temporal temperature distributions for 150mA pulse . 24 2.10 Example of raw data passed through the skeletonization algorithm to reduce the image to 41 points (x,y pixel locations) along the body of the worm. 26 2.11 Examples of raster plots generated from high-content phenotyping tool . 29 2.12 Examples of uses for high-content phenotyping tool . 30 2.13 Analysis of center-of-skeleton trajectory of a worm crawling on an agar plate, stimulated with a noxious thermal pulse at the head. 33 2.14 Normalized (z-scores) of behavioral feature vectors for 16 strains for head, midbody, and tail stimulation. 35 x 2.15 Correlation amongst strains using feature vectors from Figure 2.14. 36 3.1 Assay for the spatial dissection of the thermal noxious response.
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