UCLA UCLA Electronic Theses and Dissertations Title Analysis of the Neural and Glial Lineages Establishing the Cytoarchitecure of the Drosophila melanogaster Central Brain Permalink https://escholarship.org/uc/item/88c9q8fp Author Omoto, Jaison Jiro Publication Date 2017 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA Los Angeles Analysis of the Neural and Glial Lineages Establishing the Cytoarchitecure of the Drosophila melanogaster Central Brain A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Molecular, Cell, and Developmental Biology by Jaison Jiro Omoto 2017 © Copyright by Jaison Jiro Omoto 2017 ABSTRACT OF THE DISSERTATION Analysis of the Neural and Glial Lineages Establishing the Cytoarchitecure of the Drosophila melanogaster Central Brain by Jaison Jiro Omoto Doctor of Philosophy in Molecular, Cell, and Developmental Biology University of California, Los Angeles, 2017 Professor Volker Hartenstein, Chair Proper central nervous system (CNS) function in vertebrates and invertebrates alike requires the sufficient production of, and suitable interaction between, different classes of neurons and glial cells. Although a large heterogeneity exists between individual cells of the CNS, one can begin dissecting its construction, and ultimately function, based on developmental principles. One such principle is the lineage concept; accumulating evidence suggests that in the CNS of the fruit fly Drosophila melanogaster, classes of cells can be defined based on their progenitor origin, or lineage. Neurons and/or glial cells which derive from an individual progenitor, of which there are approximately 100 per brain hemisphere, exhibit common structural properties. In this dissertation we describe the lineage relationship, and resultant characteristics, of Drosophila brain cells in two contexts: glial cells populating the ii neuropil-cortex interface (neuropil glia) and ensembles of neurons transmitting visual information to a higher-order brain region called the central complex (Anterior Visual Pathway). In the first context, we find that astrocyte-like glial cells (ALGs), a neuropil glia subtype reminiscent of vertebrate astrocytes, are generated in two distinct waves. The first wave results from the proliferation of embryonic progenitors in the basal brain, and produces the mature ALGs of the larval brain. ALGs of the adult brain, produced during the second wave, are generated from a completely separate population of progenitors in the larva. We also characterize the cytology of these glial populations. In the second context, we find that all ring neurons of the ellipsoid body, a subcompartment of the central complex, are generated from a single lineage called DALv2. Ring neurons are a peculiar neuronal class which has been previously shown to respond to visual stimuli and are required for higher-order visually-guided behaviors. We identify two further lineages, DALcl1 and 2, which generate parallel ensembles of neurons providing visual input to ring neurons. Importantly, neurons of DALcl1 and 2 are not only developmentally-distinct, but also exhibit structural and functional differences, highlighting the rarely demonstrated principle that functional neuronal circuitry can be mapped to developmental cell lineage. Taken together, this thesis validates the utility of employing the lineage principle to formulate hypotheses of circuit function and nervous system assembly in general. iii The dissertation of Jaison Jiro Omoto is approved. Alvaro Sagasti Frank A. Laski David E. Krantz Volker Hartenstein, Committee Chair University of California, Los Angeles 2017 iv DEDICATION For Family, Friends, the Humble Fly, and Jasna v TABLE OF CONTENTS Abstract of the Dissertation .............................................................................................. ii Committee ....................................................................................................................... iv Dedication ....................................................................................................................... v Table of Contents ............................................................................................................ vi List of Figures and Tables .............................................................................................. vii Acknowledgements ....................................................................................................... viii VITA ................................................................................................................................ xi Introduction Part 1 Nervous system structure and function from the perspective of cell lineage: an overview ....................................................................... 1 References ................................................................................................................. 11 Introduction Part 2 Origins of glial cell populations in the insect nervous system. ....... 17 Figures ....................................................................................................................... 28 References ................................................................................................................. 37 Chapter One Origin and development of neuropil glia of the Drosophila larval and adult brain: Two distinct glial populations derived from separate progenitors. ................................................................................... 44 Introduction ................................................................................................................ 45 Materials and Methods ............................................................................................... 50 Results ....................................................................................................................... 54 Discussion.................................................................................................................. 67 Figures ....................................................................................................................... 77 References ............................................................................................................... 101 Chapter Two Visual input to the Drosophila central complex by developmentally and functionally distinct neuronal populations ............................ 110 Introduction .............................................................................................................. 112 Materials and Methods ............................................................................................. 116 Results ..................................................................................................................... 119 Discussion ............................................................................................................... 129 Figures ..................................................................................................................... 135 References .............................................................................................................. 152 Chapter Three Development of the anterior visual pathway to the Drosophila central complex ........................................................................... 158 Introduction .............................................................................................................. 159 Materials and Methods ............................................................................................. 163 Results ..................................................................................................................... 166 Discussion ............................................................................................................... 177 Figures ..................................................................................................................... 187 References .............................................................................................................. 203 vi LIST OF FIGURES AND TABLES INTRODUCTION Figure Intro-1 28 Figure Intro-2 30 Figure Intro-3 32 Figure Intro-4 35 CHAPTER ONE Table 1-1 77 Figure 1-1 78 Figure 1-2 81 Figure 1-3 84 Figure 1-4 86 Figure 1-5 88 Figure 1-6 90 Figure 1-7 92 Figure 1-8 94 Figure 1-9 96 Figure 1-10 98 Figure 1-11 100 CHAPTER TWO Figure 2-1 135 Figure 2-2 138 Figure 2-3 141 Figure 2-4 144 Figure 2-5 146 Figure 2-6 149 CHAPTER THREE Figure 3-1 187 Figure 3-2 188 Figure 3-3 191 Figure 3-4 193 Figure 3-5 195 Figure 3-6 197 Figure 3-7 199 Figure 3-8 201 vii ACKNOWLEDGEMENTS Thank you to Mr. Drew Lord, for showing me the door of science. Thank you to Dr. Sepehr Eskandari, for providing me a path beyond that door. Thank you to Dr. Volker Hartenstein, for swarming me with flies while on that path. Introduction Part 1 Introduction Part 1 is an overview of nervous system structure and function from the perspective of cell lineage. This work was supported by grants from the National Institutes of Health (grant number R01 NS29357-15) and the University of California, Los Angeles (Dissertation Year Fellowship). Contribution: Jaison J. Omoto wrote the manuscript. Introduction Part 2 Introduction Part 1 is adapted from Omoto et al. “Origins of glial cell populations in the insect nervous system.” (2016). Curr. Opin. Insect Sci.