The Development and Assembly of the Drosophila Adult Ventral Nerve Cord

Available online at www.sciencedirect.com ScienceDirect The development and assembly of the Drosophila adult ventral nerve cord Lalanti Venkatasubramanian and Richard S Mann In order to generate complex motor outputs, the nervous animals respond to their environments by executing system integrates multiple sources of sensory information that motor outputs. ultimately controls motor neurons to generate coordinated movements. The neural circuits that integrate higher order In order to carry out these functions, the nerve cord is commands from the brain and generate motor outputs are composed of a large number of neurons that can be located in the nerve cord of the central nervous system. classified according to their function and morphology. Recently, genetic access to distinct functional subtypes that These include local interneurons that modulate and make up the Drosophila adult ventral nerve cord has generate rhythmic motor patterns, ascending and des- significantly begun to advance our understanding of the cending neurons that relay information to and from the structural organization and functions of the neural circuits brain, and motor neurons that synapse onto muscles and coordinating motor outputs. Moreover, lineage-tracing and are directly responsible for causing muscle contractions genetic intersection tools have been instrumental in and movements. In addition, the nerve cord receives deciphering the developmental mechanisms that generate and numerous inputs from peripheral sensory neurons. As assemble the functional units of the adult nerve cord. Together, will be highlighted below, these populations can be the Drosophila adult ventral nerve cord is emerging as a further subdivided based on their specific functions powerful system to understand the development and function and anatomy. of neural circuits that are responsible for coordinating complex motor outputs. To assemble complex neural circuits, biological systems employ a range of developmental mechanisms Address that regulate and specify the number, birth order and Department of Biochemistry and Molecular Biophysics, Department of Neuroscience, Zuckerman Mind Brain Behavior Institute, unique identities of the component neurons. To link Columbia University, New York, NY 10027, United States the developmental origins of neural circuits with their functional outputs, it is advantageous to use a model Corresponding author: Mann, Richard S ([email protected]) where sophisticated tools are available for both types of analyses. The Drosophila model system is well Current Opinion in Neurobiology 2019, 56:135–143 renowned for the range of genetic tools available to dissect the development and functions of individual This review comes from a themed issue on Neuronal identity and small groups of neurons [1–5]. Moreover, adult Edited by Sacha Nelson and Oliver Hobert Drosophila execute a large range of complex motor outputs using multi-jointed legs for walking and groom- ing, and wings and halteres for flying. Additional behaviors that use these appendages are courtship by males https://doi.org/10.1016/j.conb.2019.01.013 and aggression between individuals. Notably, rudimen- tary forms of some motor programs, including walking, 0959-4388/ã 2019 Elsevier Ltd. All rights reserved. can be executed in the absence of a brain, indicating the autonomy of the circuits in the nerve cord for executing rhythmic motor outputs [6 ,7]. However, intact adult Drosophila simultaneously integrate visual, chemosen- sory, and proprioceptive inputs while executing these Introduction motor behaviors [8]. The combination of behavioral The central nervous systems of most bilaterian animals complexity, plasticity, and abundance of genetic tools can be divided into two major components, an anterior sets this system apart as an exceptionally powerful brain and a more posterior nerve cord. From among its model to understand the development and function most primitive forms in annelids, to the complex spinal of neural circuits. cord found in vertebrates, the primary function of the Drosophila nerve cord is to integrate and process information from In , most of the neurons that make up the nerve the brain to produce coordinated locomotor outputs by cord, known as the ventral nerve cord (VNC) due to its controlling muscle activities in the periphery. Under- ventral position, are born post-embryonically in the larval standing the development and assembly of circuits in stages in an immature form [9]. Because the larval and the nerve cord is, therefore, crucial for understanding how adult stages execute significantly different behaviors, the www.sciencedirect.com Current Opinion in Neurobiology 2019, 56:135–143 136 Neuronal identity Figure 1 Descending (a) D V (b) (c) Leg Motor Neurons Leg Sensory Neurons Ascending Pr Fo oN Motor re p G - V P le Pro A C g C Sensory Np mVAC Neck AMNp Am Depressor Np Chordotonal M e M s Lower-Tectulum id o - N Wing le Meso p V g A C Np Tectulum Haltere Levator Hair Plate M e V H ta A in C d N - p le Meta g Np ANp ANp Bristle Long Tendon Long Tendon (d) (e) (f) Wing Motor Neurons Descending Neurons Neuropil Glia Surface Interior MTD Astrocyte hg1 ps1 Surface Interior VLT Ensheathing (g) Wing and Haltere (h) Sensory Neurons Mesothoracic Triangle Neurons vPR6 dPR1 vms11 Current Opinion in Neurobiology Structural and functional organization of the Drosophila adult VNC. (a) Frontal (left) and lateral (right) views of the Drosophila adult VNC depicting five major neuropils — prothoracic, mesothoracic and metathoracic neuropils corresponding to the three thoracic segments and the accessory mesothoracic neuropil (AMNp), and abdominal neuropil (ANp). For nomenclature refer to Ref. [19]. Left — Neuronal subtypes projecting in and out of the Drosophila adult VNC with information flow depicted in the form of arrows. Motor and ascending neurons project axons out of the VNC (red arrows); sensory and descending neurons project into the VNC (green arrows); and Central Pattern Generator (CPG) neurons are local interneurons contained within the VNC (grey arrows). Current Opinion in Neurobiology 2019, 56:135–143 www.sciencedirect.com The Drosophila nerve cord Venkatasubramanian and Mann 137 nervous system undergoes a striking transformation dur- during the course of metamorphosis [20]. Specifically, ing metamorphosis during which adult-specific neural most adult VNC neurons arise during post-embryonic circuits develop into their mature forms. In comparison neurogenesis from 25 distinct neuroblast (NB) progeni- to the adult brain of Drosophila [10–14] much less is tors in each thoracic neuromere, and each lineage gives known about the functional organization and develop- rise to both Notch-ON and Notch-OFF hemilineages, ment of distinct adult VNC circuits. In this review we some of which undergo programed cell death [9,21]. Of highlight recent studies that begin to describe the diverse the 33 hemilineages that survive apoptosis, each extends population of cell types and neuropils that make up the primary neurites into specific tracts with stereotyped Drosophila adult VNC together with the specific tools and points of entry into an immature neuropil. These tracts, techniques that enable a more thorough understanding of readily discerned by Neuroglian staining, remain tightly their developmental origins and functional contributions fasciculated and largely intact throughout metamorpho- to various motor outputs. sis, thereby providing a consistent reference for neuropil organization. For example, certain lineage tracts define Structural and functional organization of the the boundaries of two smaller neuropils — the accessory Drosophila adult VNC mesothoracic neuropil (AmNp), which receives wing In order to understand how distinct neurons find their sensory afferents, and a dorsal compartment called the place in a functional circuit, it is crucial to characterize the tectulum, which consists of intersegmental projecting anatomy and organization of the nervous tissue. This hemilineages (Figure 1a). Interestingly, this hemiline- involves identifying specific landmarks, such as groups age-based organization of VNC anatomy is likely to be of neuronal cell bodies, neuronal tracts and commissures, functionally relevant as distinct hemilineages represent functional ‘modules’ that contribute to specific motor anatomically distinct neuropils, and the organization of non-neuronal glial cells, which contribute to the assem- outputs [6 ] (Table 2). bly, growth, and homeostasis of nervous tissue [15,16]. According to the detailed description of the anatomy of Drosophila In the insect nerve cord, neuronal cell bodies are located the adult VNC and associated nerves, the adult VNC is currently viewed as containing sixteen distinct in an outer cortex, while their projections converge into densely packed neuropils that can be recognized by neuropils [22 ] (Figure 1a, Table 1). The definition of staining for Bruchpilot and N-cadherin, two well-estab- these neuropils and their anatomical boundaries has lished markers of mature synapses [17,18]. Further, depended on multiple complementary efforts to charac- tightly fasciculated nerve bundles enter and exit specific terize the function and development of the diverse neuropils through distinct tracts and commissures, which populations of cell-types that project into the VNC are clearly identified by anti-Tubulin and anti-Futsch (Figure 1b–h). These include, but are not restricted to, Drosophila the motor neurons (MNs) controlling movements of the staining. Notably, the

Load more