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A Neuronal Circuit Architecture for Angular Integration in Drosophila Jonathan Green Rockefeller University Digital Commons @ RU Student Theses and Dissertations 2017 A Neuronal Circuit Architecture for Angular Integration in Drosophila Jonathan Green Follow this and additional works at: http://digitalcommons.rockefeller.edu/ student_theses_and_dissertations Part of the Life Sciences Commons Recommended Citation Green, Jonathan, "A Neuronal Circuit Architecture for Angular Integration in Drosophila" (2017). Student Theses and Dissertations. 405. http://digitalcommons.rockefeller.edu/student_theses_and_dissertations/405 This Thesis is brought to you for free and open access by Digital Commons @ RU. It has been accepted for inclusion in Student Theses and Dissertations by an authorized administrator of Digital Commons @ RU. For more information, please contact [email protected]. A NEURONAL CIRCUIT ARCHITECTURE FOR ANGULAR INTEGRATION IN DROSOPHILA A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy by Jonathan Green June 2017 ã Copyright by Jonathan Green 2017 A NEURONAL CIRCUIT ARCHITECTURE FOR ANGULAR INTEGRATION IN DROSOPHILA Jonathan Green, Ph.D. The Rockefeller University 2017 While navigating their environment, many animals keep track of their angular heading over time. However, a neuronal-circuit architecture for computing heading remains unknown in any species. In this thesis, I describe a set of neurons in the Drosophila central complex whose wiring and physiology provide a means to shift an angular heading estimate when the fly turns. I show that these clockwise- and counterclockwise-shifting neurons each exist in two subtypes, with spatiotemporal activity profiles that suggest opposing roles for each subtype at the start and end of a turn. Shifting neurons are required for the heading system to properly track the fly's heading in the dark, and their stimulation induces a shift in the heading signal in the expected direction. I also provide evidence that the angular position of visual landmarks is flexibly associated with the fly’s internal heading estimate as it explores its environment. A specific circuit-level model based on known cell types is proposed to account for this flexible association. The central features of the biological circuits described here are analogous to computational models proposed for head- direction cells in rodents and may inform how neural systems, in general, perform angular calculations. Acknowledgments I wish to thank Gaby Maimon, my supervisor, for teaching me most of what I know in neuroscience, for his willingness to grant perhaps unwarranted freedom, and most importantly, for his unwavering support over many years without success. It would be an understatement to say that this project would not have been possible without his guidance. I wish to thank Atsuko Adachi, who tirelessly dissected, stained and imaged a seemingly endless list of fly brains. All immunohistochemistry experiments, as well as the comprehensive tracing of P-EN neurons, were entirely her work. Atsuko also helped with fly genetics. I wish to thank Kunal Shah for his skill and patience in fine tuning the fabrication of new fly holders down to the last (50) micron, as well as designing and machining various parts for the experimental rig. Thanks to Pablo Magani, who tested various sphere-tracking methods, and finally discovered and set up FicTrac to operate in closed loop in our system. Thanks to Jonathan Hirokawa for, among many things, developing a pipeline for registering imaging data. I wish to thank Christoph Kirst, who introduced me to the world of neuronal network models; Vikram Vijayan, who had the initial idea of using Gal4 lines from the Flood et al. 2013 TrpA1 screen as a starting point for a P2X2 screen; and all members of the Maimon Lab for thoughtful discussions and general help over the years. iii I wish to thank the members of my committee: Sandy Simon, Cori Bargmann and Vanessa Ruta, for helpful feedback and their support and interest over the years. Thanks to the Ruta and Rubin labs for fly stocks, and the DiAntonio and Krantz labs for antibodies. Finally, I wish to thank Saša Jereb, my other half, and my friends and family, for making a lopsided person slightly less lopsided. iv Table of Contents Acknowledgments iii List of Figures vi List of Tables viii Chapter 1 | Introduction 1 Chapter 2 | Identifying turning-related neurons 27 Chapter 3 | A neuronal circuit architecture for angular integration 43 Chapter 4 | Flexibly learning angular landmark positions. 106 Chapter 5 | Discussion 125 Methods 156 References 178 v List of Figures Figure 1.1 | Rats flexibly navigate towards their goal. 5 Figure 1.2 | Neuronal model proposed for head direction cells in Skaggs et al. 1995. 22 Figure 2.1 | P-ENs are a main component of NP0212-labeled neurons in the protocerebral bridge. 30 Figure 2.2 | Finding turning-related neurons through a stimulation screen. 33 Figure 2.3 | Initial characterization of an asymmetric and periodic signal in the protocerebral bridge. 38 Figure 3.1 | The activity of three cell types in the bridge tracks the fly’s heading. 46 Figure 3.2 | Processing of protocerebral bridge signals from E-PG, P-EN1 and P- EN2 neurons in the presence of a closed-loop bar. 47 Figure 3.3 | Processing of protocerebral bridge signals from E-PG, P-EN1 and P- EN2 neurons in the dark. 49 Figure 3.4 | Example visual tuning curves in E-PG, P-EN1 and P-EN2 neurons across glomeruli in the protocerebral bridge. 51 Figure 3.5 | P-EN neurons in the left and right bridge are asymmetrically active when the fly turns, consistent with an anatomically-inspired model for neural integration. 54 Figure 3.6 | P-EN neuroanatomy: explanation for the numbering scheme, sytGFP localization, and multicolor single cell labeling. 56 Figure 3.7 | P-EN1 and P-EN2 bridge asymmetry during turns in closed-loop bar and dark conditions, computed with z-score and ∆F/F normalizations. 61 Figure 3.8 | P-EN1 and P-EN2 asymmetries are driven in part by optic flow. 63 vi Figure 3.9 | The P-EN1 activity peak leads, and the P-EN2 peak trails, a rotating E-PG peak in the ellipsoid body, as predicted by their activity in the bridge. 69 Figure 3.10 | Co-labeling of P-EN1 and P-EN2 driver lines. 71 Figure 3.11 | Simultaneous imaging of the protocerebral bridge and ellipsoid body for each cell type separately and dual-color imaging of GCaMP6f and jRGECO1a in E-PGs in the ellipsoid body. 72 Figure 3.12 | Analysis of the ellipsoid body asymmetry in P-EN1s and P-EN2s relative to E-PGs in the ellipsoid body. 73 Figure 3.13 | Timing of P-EN1 and P-EN2 bridge asymmetries. 76 Figure 3.14 | The effect of blocking P-EN synaptic transmission on the E-PG phase in the dark. 78 Figure 3.16 | P-EN neurons medially excite E-PG neurons in the bridge, consistent with a model for neural integration. 83 Figure 3.17 | Controls for the P2X2 experiments. 84 Figure 3.19 | Flies turn in response to a stimulated change in the heading signal. 86 Figure 3.20 | Total bridge activity increases during walking. 92 Figure 4.1 | E-PG properties during closed-loop bar 107 Figure 4.2 | Circuit architectures for mapping landmarks to a heading signal 110 Figure 4.3 | Stability of the mapping between E-PG phase and bar position 117 Figure 5.1 | A framework for building a heading signal with known cell types. 132 Figure 5.2 | Similarities between models for the fly and rat heading systems 146 Figure 5.3 | Model for behavioral control of heading 153 vii List of Tables Table 3.1 | Characterization and classification of individual neurons identified by multi color flip out in three P-EN Gal4 lines. 101 viii Chapter 1 | Introduction Animals everywhere are navigating. The arctic tern migrates from the south to the north pole (Egevang et al. 2010), sea turtles swim across the Atlantic Ocean (Fuxjager, Eastwood, and Lohmann 2011), and monarch butterflies fly between Canada and Mexico (Reppert, Gegear, and Merlin 2010). Humbler animals navigate over shorter distances, but with no less importance to their survival. For example, honeybees direct each other towards a source of nectar (von Frisch 1967). After finding food during a meandering outbound search from the nest, ants can walk directly back home (Wehner and Srinivasan 2003). At the heart of each of these complex navigational routes is the basic computation of “where am I heading?”. The first step towards a neurobiological understanding of this computation came with the discovery of head direction cells in rats (Taube, Muller, and Ranck 1990a). More recently, evidence for heading-sensitive cells has emerged in other species (Varga and Ritzmann 2016; Heinze and Homberg 2007; Finkelstein et al. 2015), including Drosophila (Seelig and Jayaraman 2015) (heading is used here to refer more ambiguously to the animal’s orientation, without specifying head direction or body direction, since in some cases – as in when the animal’s head and body are tethered - the two cannot be distinguished). However, the neuronal mechanisms that build these heading signals remain unknown in any species. This thesis characterizes how a neuronal circuit in the fruit fly, Drosophila melanogaster, computes the fly’s heading. 1 To frame these results within the broader context of spatial navigation, I first review the behavioral evidence for the existence of an internal sense of heading and space in animals. Second, I review the physiology of neuronal systems that respond specifically to navigational variables, including head- direction. Finally, I review the neural network models that have been proposed to explain how the physiological properties of head-direction cells and other spatially-responsive neurons are constructed from more basic inputs.
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