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The Astrocyte Network in the Ventral Nerve Cord Neuropil of the Drosophila Third-Instar Larva

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The Astrocyte Network in the Ventral Nerve Cord Neuropil of the Drosophila Third-Instar Larva The astrocyte network in the ventral nerve cord neuropil of the Drosophila third-instar larva Item Type Article Authors Hernandez, Ernesto; MacNamee, Sarah E; Kaplan, Leah R; Lance, Kim; Garcia-Verdugo, Hector D; Farhadi, Dara S; Deer, Christine; Lee, Si W; Oland, Lynne A Citation Hernandez, E, MacNamee, SE, Kaplan, LR, et al. The astrocyte network in the ventral nerve cord neuropil of the Drosophila thirdinstar larva. J Comp Neurol. 2020; 1– 21. https:// doi.org/10.1002/cne.24852 DOI 10.1002/cne.24852 Publisher WILEY Journal JOURNAL OF COMPARATIVE NEUROLOGY Rights © 2020 Wiley Periodicals, Inc. Download date 29/09/2021 07:02:47 Item License http://rightsstatements.org/vocab/InC/1.0/ Version Final accepted manuscript Link to Item http://hdl.handle.net/10150/636762 The astrocyte network in the ventral nerve cord neuropil of the Drosophila third-instar larva Running title: Drosophila VNC astrocyte network Ernesto Hernandez1,2, Sarah E. MacNamee1,3, Leah R. Kaplan1,4, Kim Lance1, Hector D. Garcia- Verdugo1, Dara S Farhadi1,5, Christine Deer1,6, Si Woo Lee1, Lynne A. Oland1 Current addresses: 2Hernandez: University of Illinois at Chicago School of Medicine, 1601 Parkview Ave, Rockford, IL 61107; [email protected] 3MacNamee: Inscopix, 2452 Embarcadero Way, Palo Alto, CA 94303 4Kaplan: Consortium for Science, Policy & Outcomes, Arizona State University, 1800 I St NW, Suite 300, Washington, DC 20006 5Farhadi: University of Arizona, College of Medicine – Phoenix, 475 N 5th St, Phoenix, AZ 85004 6Deer: University of Arizona, University Information Technology Service, Research Technologies Group, Data Visualization Team Corresponding author: Lynne A. Oland, Ph.D. Department of Neuroscience University of Arizona PO Box 210077 Tucson, AZ 85721-0077 520-621-7215 [email protected] Data Sharing: The data that support the findings of this study are available from the corresponding author upon reasonable request. Acknowledgements: The authors are deeply grateful to Patty Jansma of the University of Arizona’s Core Imaging Facility who guided our students in use of the confocal and multi- photon microscopes; to Mark Borgstrom of the UITS Statistics Consultation Team who guided our statistical analyses; to Anu Sethuraman, a high school student who began the analysis of cross-segmental arborization; to Cathy Tran, who as an undergraduate carried out many of our immunocytochemistry experiments; and to Leslie Tolbert, who always provided insightful review and guidance of the work in this paper. The image rendering work was funded by University Information Technology Systems (UITS), Research Technologies Group, Visualization Team (funded by Technology Research Investment Fund/Space Exploration and Optical Sciences). The study was funded by NSF, grant #IOS-1353739 to LAO. 1 Abstract Understanding neuronal function at the local and circuit level requires understanding astrocyte function. We have provided a detailed analysis of astrocyte morphology and territory in the Drosophila 3rd-instar VNC where there already exists considerable understanding of the neuronal network. Astrocyte shape varies more than previously reported; many have bilaterally symmetrical partners, many have a high percentage of their arborization in adjacent segments, and many have branches that follow structural features. Taken together, our data are consistent with, but not fully explained by, a model of a developmental growth process dominated by competitive or repulsive interactions between astrocytes. Our data suggest that the model also should include cell-autonomous aspects, as well as use of structural features for growth. Variation in location of arborization territory for identified astrocytes was great enough that a standardized scheme of neuropil division among the six astrocytes that populate each hemi- segment is not possible at the 3rd instar. The arborizations of the astrocytes can extend across neuronal functional domains. The ventral astrocyte in particular, whose territory can extend well into the proprioceptive region of the neuropil, has no obvious branching pattern that correlates with domains of particular sensory modalities, suggesting that the astrocyte would respond to neuronal activity in any of the sensory modalities, perhaps integrating across them. This study sets the stage for future studies that will generate a robust, functionally-oriented connectome that includes both partners in neuronal circuits – the neurons and the glial cells, providing the foundation necessary for studies to elucidate neuron-glia interactions in this neuropil. Key words: glial cells, neuron-glia interaction 2 glial cells, neuron-glia interaction RRID:BDSC Cat# 30125, RRID:BDSC_30125 RRID:BDSC Cat# 4775, RRID:BDSC_4775 RRID:BDSC Cat# 6938, RRID:BDSC_6938 RRID:BDSC Cat# 64085, RRID:BDSC_64085 RRID:BDSC Cat# 5692, RRID:BDSC_5692 RRID:BDSC Cat# 38760, RRID:BDSC_38760 RRID:DSHB Cat# 1D4, RRID:AB_528235 RRID:Molecular Probes Cat# 6455, RRID:AB_2314543 RRID:Jackson ImmunoResearch Labs Cat# 115-167-003, RRID:AB_2338709 RRID:Molecular Probes Cat# A-21236, RRID:AB_141725 RRID:Bio-rad Cat # MCA1360, RRID:AB_322378 RRID:Cell Signaling Technology Cat # 3724, RRID:AB_1549585 RRID:Novus Cat # NBP1-06712, RRID:AB_1625981 RRID:Abcam Cat# ab6953, RRID:AB_955010 RRID:DSHB Cat# nc82, RRID:AB_2314866 RRID:Thermo Fisher Scientific Cat# A-11034, RRID:AB_2576217 Main Text Introduction Concerted efforts toward mapping neuronal connectomes have generated rapid advances in our knowledge of brain circuitry and organization. As the number and details of various neuronal connectomes in different species increase, it is critically important that glial cells, which help determine and then regulate both anatomical and functional neuronal connectivity, be included in these maps (Corty & Freeman, 2013; Clarke & Barres, 2013; Fields, et al., 2015). Given their association with synapses and their organization into domains that may modulate local neuronal 3 activity and synaptic interactions, astrocytes are particularly well-positioned to play a role in the spatial segregation of information as well as the spread of information (Bushong, et al., 2002; Halassa, et al., 2007). Here, we have interrogated the anatomical features of astrocytes that comprise the glial network in the ventral nerve cord (VNC) neuropil of the third-instar larva. The VNC neuropil features well-described neuronal sensori-motor maps (Schrader and Merritt, 2000; Zlatic et al., 2009), and these territories are readily identifiable using FasII-positive axon tracts as anatomical landmarks (Landgraf et al., 2003b). The 3rd instar is the stage at which the bulk of studies that examine the physiology of neurons have been carried out (Choi, et al., 2004; Worrell & Levine, 2008; Heckscher, et al., 2015; Ohyama, et al., 2015; Fushiki, et al., 2016; Clark, et al., 2016; Tastekin, et al., 2018) as well as the only stage to date in which the electrophysiological characteristics of astrocytes and astrocyte-synapse interactions have been examined (MacNamee, et al., 2016.) Of the glial subtypes commonly recognized in the Drosophila CNS (Hartenstein, 2011; Freeman, 2015; Kremer, et al., 2017), here we have focused on the astrocyte-like glia. While several of the glial subtypes in Drosophila may contribute to what are the functions of astrocytes in vertebrates, including Drosophila cortex, ensheathing and astrocyte-like glia, the morphological, developmental, molecular, and functional similarities between Drosophila astrocytes and vertebrate protoplasmic astrocytes are well-documented (Freeman, 2015; Ma, et al., 2016; MacNamee, et al., 2016; Peco, et al., 2016; Yildirim, et al., 2019;). Morphologically, these species’ astrocytes share a highly branched structure, with processes that are strikingly complex and include veil-like distal processes (leaflets) found in the vicinity of neuronal synapses. During development, both vertebrate astrocytes and Drosophila astrocytes participate in the formation of synaptic networks by regulating synaptogenesis (Eroglu, et al., 2009; Molofsky, et al., 2012; 4 Allen, et al., 2012; Muthukumar, et al., 2014; Stork, et al., 2014) and by pruning synaptic spines (MacDonald et al., 2006; Doherty, et al., 2009; Chung, et al., 2013). They contribute to the determination of neuronal cell number and can promote, prune and/or dynamically regulate synaptic connectivity through various mechanisms (vertebrates: Eroglu & Barres, 2010; invertebrates: Corty & Freeman, 2013). In Drosophila, ablation of specific astrocytes during pupal-stage synaptogenesis has both anatomical (reduced synapse number and density) and behavioral (failed or partial eclosion) consequences (Muthukumar, et al., 2014). Astrocytes functionally regulate synaptic strength in both vertebrate and fly nervous systems (Theodosis, et al., 2008; Clark & Barres, 2013; Liu, et al., 2014; Verkhratsky & Nedergaard, 2018). Astrocytic processes reside near synapses, and Drosophila astrocytes express molecular markers that are shared with vertebrate astrocytes, including the neurotransmitter transporters Eaat1 (Rival, et al., 2004; 2006) and Gat (Muthukumar, et al., 2014). Astrocyte cell-body recordings in Drosophila show transporter-mediated responses to glutamatergic neuronal activity and cell-intrinsic physiology that is strikingly similar to that of vertebrate protoplasmic astrocytes (MacNamee, et al., 2016). Also, Drosophila astrocyte activity has been shown to regulate nervous system function at the level of synaptic signaling (Liu, et al., 2014; MacNamee, et al.,
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