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VIEW Open Access Structural Aspects of Plasticity in the Nervous System of Drosophila Atsushi Sugie1,2†, Giovanni Marchetti3† and Gaia Tavosanis3*

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VIEW Open Access Structural Aspects of Plasticity in the Nervous System of Drosophila Atsushi Sugie1,2†, Giovanni Marchetti3† and Gaia Tavosanis3* Sugie et al. Neural Development (2018) 13:14 https://doi.org/10.1186/s13064-018-0111-z REVIEW Open Access Structural aspects of plasticity in the nervous system of Drosophila Atsushi Sugie1,2†, Giovanni Marchetti3† and Gaia Tavosanis3* Abstract Neurons extend and retract dynamically their neurites during development to form complex morphologies and to reach out to their appropriate synaptic partners. Their capacity to undergo structural rearrangements is in part maintained during adult life when it supports the animal’s ability to adapt to a changing environment or to form lasting memories. Nonetheless, the signals triggering structural plasticity and the mechanisms that support it are not yet fully understood at the molecular level. Here, we focus on the nervous system of the fruit fly to ask to which extent activity modulates neuronal morphology and connectivity during development. Further, we summarize the evidence indicating that the adult nervous system of flies retains some capacity for structural plasticity at the synaptic or circuit level. For simplicity, we selected examples mostly derived from studies on the visual system and on the mushroom body, two regions of the fly brain with extensively studied neuroanatomy. Keywords: Structural plasticity, Drosophila, Photoreceptors, Synapse, Active zone, Mushroom body, Mushroom body calyx, Learning Background neuronal types, the feed-back derived from activity ap- The establishment of a functional neuronal circuit is a pears to be an important element to define which connec- dynamic process, including an extensive structural re- tions can be stabilized and which ones removed [3–5]. modeling and refinement of neuronal connections. Nonetheless, the cellular mechanisms initiated by activity Intrinsic differentiation programs and stereotypic mo- to drive structural remodeling during development and in lecular pathways contribute the groundwork of pattern- the course of adult life are not fully elucidated. Here, we ing the nervous system during development, including review the literature supporting structural plasticity in the the guidance of axons and dendrites over long distances fruit fly Drosophila, a system offering major advantages or the recognition of appropriate connection partners. for genetic and molecular analysis. Where appropriate, we In addition, information derived from functional cues include comparisons with other invertebrate and verte- controls the refinement of the circuit. Even after the brate systems to highlight evolutionary conserved mecha- major task of assembling a fully functional network has nisms. Thanks to the stereotypy of the “macroscopic” been achieved, the nervous system retains the capacity organization of the fly’s nervous system, work carried out of undergoing not only functional, but also structural using Drosophila led to major breakthroughs in the identi- modifications related, for instance, to adaptation or fication of conserved molecular cascades and mechanisms learning. The role of activity in the developmental re- that orchestrate genetically controlled developmental pro- finement of neuronal morphology and of the connec- grams. Possibly due to this emphasis on stereotypy, the tions within a circuit (and possibly also the setting up of role of signals providing feed-back information about circuits; [1]) as well as in the initiation of structural re- functional connections during fly nervous system develop- modeling during adult life is undisputed [2]. In intricate ment has not been investigated as deeply. Nonetheless, neuropils, dense with axons and dendrites of different multiple examples of activity controlling neuronal com- plexity during development have emerged [6]. For in- stance, dendrite elaboration of fly larval motorneurons as * Correspondence: [email protected] †Atsushi Sugie and Giovanni Marchetti contributed equally to this work. well as of the wide-field serotonergic neuron CSDn in the 3Center for Neurodegenerative Diseases (DZNE), 53127 Bonn, Germany Drosophila central nervous system can be affected by the Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sugie et al. Neural Development (2018) 13:14 Page 2 of 11 level of input signals and actually by input activity during molecular components of the synapse [33, 34]. In this re- development [7, 8]. Similarly, exposure of the larva to dif- view we will select the aspects that deal in particular with ferent light regimes modifies the total dendrite length of the structural components of functional and synaptic plas- ventral lateral neurons (LNv), postsynaptic to the photore- ticity. We chose to focus on two centers of the fly nervous ceptors [9]. The accessibility of the neuromuscular junction system to summarize the current evidence in support of (NMJ) of larvae allows for detailed molecular, morpho- an influence of activity during development and of plastic logical and functional analysis [10]. The level of activity in changes in the adult nervous system in adaptive or the motorneuron can modulate the number of boutons learning conditions. formed and the density of synaptic release sites at the NMJ, providing a clear example of activity-related structural con- The establishment of circuits trol [11–13]. In this context, postsynaptically-derived sig- The ease of manipulating their input makes sensory nals carried by the Wnt and BMP signaling pathways, systems particularly suitable for the study of activity- modulate the presynaptic terminal at the NMJ [14–16]. dependent processes involved in neuronal circuit assem- Evidence for structural rearrangements in the nervous bly, refinement and plasticity. In this review we concen- system of the adult fly after development is completed trate therefore our attention on the fly adult visual system has been rather limited and it is mostly related to adap- and on the pathways that deliver olfactory information to tive phenomena. As an example, prolonged exposure to the mushroom body (MB), involved in memory processing. a given odor induces increased size and synaptic density Sensory information is initially encoded in discrete in discrete glomeruli of the antennal lobe, the first olfac- stereotypic pathways. For instance, the presence of a tory processing center [17, 18]. Nonetheless, the behav- bright signal in the visual field or the specific odorant ior of adult flies (as well as of larvae) can be modified by present in the air flux activates defined subroutines experience in a non-adaptive fashion. In fact, flies can within the visual or olfactory circuits, respectively. To learn multiple types of cues and form lasting memories, maintain the initial specificity of information and to a capacity that might require structural modifications in transmit it precisely towards higher processing centers, the neurons and the circuits involved [19–21]. circuits are assembled with remarkable precision during Recent large-scale efforts are yielding complete maps development. Correct axon and dendrite targeting to the at synaptic-resolution of circuits within the adult fly cen- appropriate region, pairing of the suitable synaptic tral nervous system, including areas involved in memory partners and synaptogenesis are all highly regulated formation [22, 23]. This information can be combined developmental steps (Fig. 1). In principle, targeting and with the availability of tools to visualize, manipulate and recognition of processes to form functional connections control the activity of restricted and defined populations can be achieved through genetically defined pathways. of neurons in this system [24–27]. Thus, novel insights For instance, specific tags and receptors allow the cor- to the fundamental understanding of information pro- rect partner neurons to recognize each other. Alterna- cessing and of learning are starting to be produced and tively, guidance signals could support the formation of much more is expected in the coming years [22, 28–30]. initially sloppy maps, which are subsequently refined. In Importantly, the high-resolution description of circuits this case, the evaluation of the functional performance obtained in electron microscopy images and with tools of a given connection or of the circuit is likely to be a to highlight synaptic components is challenging the idea highly valuable factor for deciding whether the connec- of circuit stereotypy in the fly nervous system. As an ex- tion should be maintained or removed [35]. ample, the detailed study of motorneuron network in Here, we address how much these two potential mecha- the ventral nerve cord of the larva revealed a high de- nisms contribute to the assembly of circuits in the visual gree of variability in terms of synaptic connections [31]. system or in the MB. While the extant literature regarding Taken together, it appears that it is the right time to the molecular mechanisms of genetically controlled pro- approach the non-stereotypy and
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