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1 Nociceptive Interneurons Control Modular Motor Pathways to Promote 1 Nociceptive interneurons control modular motor pathways to promote escape 2 behavior in Drosophila 3 4 Anita Burgos1,*, Ken Honjo2, Tomoko Ohyama3, Cheng Sam Qian1, Grace Ji-eun Shin10, 5 Daryl M. Gohl4, Marion Silies5, W. Daniel Tracey6,7, Marta Zlatic8, Albert Cardona8, 6 Wesley B. Grueber1,10,11,* 7 8 9 Running title: 10 Nociceptive interneurons in Drosophila 11 12 Affiliations 13 1Department of Neuroscience, Columbia University Medical Center, New York, NY 14 10032, USA 15 16 2Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 17 305-8572, Japan 18 19 3Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada 20 21 4University of Minnesota Genomics Center, 1-210 CCRB, Minneapolis, MN 55455, USA 22 23 5European Neuroscience Institute Göttingen, Grisebachstr. 5, 37077, Göttingen, Germany 24 25 6The Linda and Jack Gill Center for Biomolecular Science, Indiana University, 26 Bloomington, IN 47405-7005, USA 27 28 7Department of Biology, Indiana University, Bloomington, IN 47405-7005, USA 29 30 8Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147, USA 31 1 32 10Department of Physiology and Cellular Biophysics, Columbia University Medical 33 Center, New York, NY 10032, USA 34 35 11Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New 36 York, NY 10032, USA 37 38 *Contact information: [email protected]; [email protected] 39 2 40 41 Abstract 42 Rapid and efficient escape behaviors in response to noxious sensory stimuli are essential 43 for protection and survival. Yet, how noxious stimuli are transformed to coordinated 44 escape behaviors remains poorly understood. In Drosophila larvae, noxious stimuli 45 trigger sequential body bending and corkscrew-like rolling behavior. We identified a 46 population of interneurons in the nerve cord of Drosophila, termed Down-and-Back 47 (DnB) neurons, that are activated by noxious heat, promote nociceptive behavior, and are 48 required for robust escape responses to noxious stimuli. Electron microscopic circuit 49 reconstruction shows that DnBs are targets of nociceptive and mechanosensory neurons, 50 are directly presynaptic to pre-motor circuits, and link indirectly to Goro rolling 51 command-like neurons. DnB activation promotes activity in Goro neurons, and 52 coincident inactivation of Goro neurons prevents the rolling sequence but leaves intact 53 body bending motor responses. Thus, activity from nociceptors to DnB interneurons 54 coordinates modular elements of nociceptive escape behavior. 55 56 3 57 Introduction 58 Nociception promotes the avoidance of harmful stimuli, and is a fundamental and 59 evolutionarily conserved somatic sense. Although the sensory neurons that detect noxious 60 stimuli have been well studied in numerous organisms, how noxious stimuli are 61 transformed to the complex sequence of behaviors that protect animals from harm 62 remains poorly understood. A key goal is to integrate anatomical, connectivity, and 63 behavioral data to provide a comprehensive view of nociceptive circuit function. 64 Drosophila larvae provide an advantageous system in which to dissect 65 nociceptive circuit organization, connectivity and function. Dendritic arborization (da) 66 sensory neurons extend axon terminals to discrete locations of the ventral nerve cord in a 67 modality specific manner (Grueber et al., 2007; Merritt and Whitington, 1995; Todd, 68 2010). The stereotypical projections of da sensory axons, characterization of da neuron 69 function, and accessibility of central neurons afforded by large collections of Gal4 lines 70 (Gohl et al., 2011; Jenett et al., 2012; Li et al., 2014) permit dissection of somatosensory 71 circuit organization. 72 Class IV (cIV) da neurons are polymodal nociceptive neurons with receptive 73 territories that together tile the entire larval epidermis (Grueber et al., 2002; Hwang et al., 74 2007; Xiang et al., 2010). cIV neural activity is both necessary and sufficient for 75 generating defensive withdrawal (nocifensive) behavior in response to noxious stimuli 76 (Hwang et al., 2007). Strong mechanical and high thermal stimulation induce C-shaped 77 body bending and corkscrew-like lateral turning (rolling) behavior, followed by rapid 78 forward locomotion, or escape crawl (Hwang et al., 2007; Ohyama et al., 2013; Tracey et 79 al., 2003). The behavioral responses of Drosophila larvae to noxious stimuli are thus both 80 diverse and sequential, suggesting complexity in the circuits downstream of primary 81 sensory neurons. Electron microscopic (EM) reconstruction of ventral nerve cord 82 circuitry has identified circuit elements downstream of cIV neurons, including Basin and 83 Goro neurons, that integrate vibration and noxious stimuli (Ohyama et al., 2015). Basin 84 cells receive multiple sensory inputs in distinct regions of the arbor, and impinge on the 85 command-like rolling Goro interneurons (Jovanic et al., 2016; Ohyama et al., 2015). 86 Although previous data suggest complexity in transduction and integration of inputs 4 87 leading to nociceptive behavior, how microcircuits promote and coordinate the rapid 88 induction of sequential stages of nociceptive behavior remains unknown. 89 Here, we identify a population of somatosensory interneurons, the Down-and- 90 Back (DnB) neurons, which arborize in the nociceptive neuropil, and receive input from 91 both nociceptive and gentle-touch sensory neurons. DnBs are activated by heat stimuli in 92 the noxious range, and their activity promotes C-shaped bending and rolling, but not 93 behaviors associated with gentle touch. EM reconstruction indicates that DnBs receive 94 almost exclusive sensory inputs, and provide major input to premotor neurons and 95 indirect input to Goro rolling command-like neurons. We find that DnBs promote the 96 activity of Goro interneurons, and that DnB-induced rolling, but not C-bending, is 97 dependent on Goro activity. Thus, studies of DnB neurons reveal a sequential and 98 modular organization of escape behavior, and a node in the nociceptive circuit that 99 coordinates essential components of nocifensive behavior to enable rapid escape 100 locomotion. 101 102 Results 103 Identification of interneurons that promote nociceptive behavior 104 To gain access to somatosensory circuitry, we examined integrase swappable in 105 vivo targeting element (InSITE) Gal4 lines (Gohl et al., 2011) for expression in the 106 ventral region of the ventral nerve cord (VNC) where class IV (cIV) nociceptive axons 107 terminate (Grueber et al., 2007)(Figure 1A). We identified two promising lines, 412-Gal4 108 and 4051-Gal4, that labeled segmental interneurons with processes in the ventromedial 109 neuropil (Figure 1B, Figure 1—figure supplement 1A). We generated 412-QF by 110 standard InSITE swapping methods (Gohl et al., 2011) and verified overlapping 111 expression of 4051-Gal4 and 412-QF in the same population of interneurons in the VNC 112 (Figure 1— figure supplement 1B-C). 412-Gal4 also labeled a bilateral population of 113 neurons in the brain lobes, and faintly labeled other cell bodies in the VNC (typically 2, 114 and up to 6, additional cells per hemisegment; Figure 1B), but did not label primary 115 sensory neurons or motor axons (Figure 1—figure supplement 2A-C'). We identified the 116 two additional neuron types consistently labeled by 412-Gal4 and 4051-Gal4 in the nerve 117 cord (Figure 1—figure supplement 2D): serotonergic A26e neurons (Huser et al., 2012; 5 118 Okusawa et al., 2014) (Figure 1—figure supplement 2E), and GABAergic A27j neurons 119 (Fushiki et al., 2016; Schneider-Mizell et al., 2016) (Figure 1— figure supplement 2F). 120 To characterize the morphology of 412-Gal4 segmental interneurons at single cell 121 resolution, we used the ‘Flip out’ technique (Basler and Struhl, 1994; Wong et al., 2002). 122 Primary neurites project to the ventromedial neuropil, where they arborize profusely 123 (Figure 1C-C'). These medial processes accumulated the dendritic marker, DenMark 124 (Nicolai et al., 2010) (Figure 1—figure supplement 3A-A'). A single process emerged 125 from this dendritic region and projected laterally and dorsally back towards the cell body 126 (Figure 1C'). These lateral projections accumulated the presynaptic marker 127 Bruchpilot.shortmCherry (BRP.shortmCherry) (Schmid et al., 2008) (Figure 1—figure 128 supplement 3B-B'). We also observed BRP.shortmCherry accumulation in medial dendrites, 129 suggesting both presynaptic and postsynaptic functions for these arbors (Figure 1— 130 figure supplement 3B-B'). Fitting with lineage-based nomenclature, the interneurons 131 labeled by 412-Gal4 were identified as the A09l neurons (Gerhard et al., 2017; Lacin and 132 Truman, 2016). Because these neurons project ‘down’ to the ventromedial neuropil, 133 arborize, and sent a reverse projection back towards the cell body, we refer to them as 134 “Down-and-Back” or DnB neurons. 135 Next, we assessed the behavioral consequences of activating 412-Gal4 neurons 136 using both thermogenetic and optogenetic approaches. Thermogenetic activation of 412- 137 Gal4 or 4051-Gal4 neurons triggered rolling behavior (Figure 1—figure supplement 4A- 138 C; Video 1). We observed similar rolling behavior when we activated 412-Gal4 neurons 139 using ReaChR (71% larvae rolling, n=48) in animals raised with all-trans-retinal, an 140 essential co-factor for channelrhodopsin (Figure 1—figure supplement 4D; Video 1). We 141 next genetically separated 412-Gal4 brain expression from VNC expression
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