Neural Basis for Looming Size and Velocity Encoding in the Drosophila Giant Fiber Escape Pathway

Ache, Jan Marek; Polsky, Jason; Alghailani, Shada; Parekh, Ruchi; Breads, Patrick; Peek, Martin Y; Bock, Davi D.; Reyn, Catherine R. von; Card, Gwyneth M

doi:10.1016/j.cub.2019.01.079

Cited by 114 publications

(173 citation statements)

References 52 publications

(92 reference statements)

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“…Many neurons connecting the OL and the central brain, or the visual projection neurons (VPNs), are identified and annotated, along with their synaptic terminals in the central brain, and in the optic lobe when possible. Among them, the columnar VPNs, including the lobula columnar (LC), lobula plate columnar (LPC), lobula-lobula plate columnar (LLPC), and lobula plate-lobula columnar (LPLC) neurons( Ache et al, 2019 )( Fischbach and Dittrich, 1989 )( Klapoetke et al, 2017 )( Otsuna and Ito, 2006 )( Wu et al, 2016 ), account for the vast majority of the population and are more or less densely identified. Since the distribution of the columnar neurons follows the arrangement of the photoreceptor cells in the compound eye, the retinotopy can be traced even in their terminals in the central brain.…”

Section: Supplemental Methodsmentioning

confidence: 99%

A Connectome and Analysis of the AdultDrosophilaCentral Brain

Scheffer

Januszewski

et al. 2020

Preprint

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The neural circuits responsible for animal behavior remain largely unknown. We 31 summarize new methods and present the circuitry of a large fraction of the brain of the fruit fly 32 Drosophila melanogaster. Improved methods include new procedures to prepare, image, align, 33 segment, find synapses in, and proofread such large data sets. We define cell types, refine 34 computational compartments, and provide an exhaustive atlas of cell examples and types, many of 35 them novel. We provide detailed circuits consisting of neurons and their chemical synapses for 36 most of the central brain. We make the data public and simplify access, reducing the effort needed 37 to answer circuit questions, and provide procedures linking the neurons defined by our analysis 38 with genetic reagents. Biologically, we examine distributions of connection strengths, neural motifs 39 on different scales, electrical consequences of compartmentalization, and evidence that 40 maximizing packing density is an important criterion in the evolution of the fly's brain. 41 1 of 57 53 Producing this data set required advances in sample preparation, imaging, image alignment, ma-54 chine segmentation of cells, synapse detection, data storage, proofreading software, and protocols 55 to arbitrate each decision. A number of new tests for estimating the completeness and accuracy 56 were required and therefore developed, in order to verify the correctness of the connectome. 57 These data describe whole-brain properties and circuits, as well as contain new methods to 58 classify cell types based on connectivity. Computational compartments are now more carefully 59 defined, we identify actual synaptic circuits, and each neuron is annotated by name and putative 60 cell type, making this the first complete census of neuropils, tracts, cells, and connections in this 61 2 of 57 Manuscript submitted to eLife Figure 2. Brain regions contained and defined in the hemibrain, following the naming conventions of (Ito et al., 2014) with the addition of (R) and (L) to specify the side of the soma for that region. Gray italics indicate master regions not explicitly defined in the hemibrain. Region LA is not included in the volume. The regions are hierarchical, with the more indented regions forming subsets of the less indented. The only exceptions are dACA, lACA, and vACA which are considered part of the mushroom body but are not contained in the master region MB.portion of the brain. We compare the statistics and structure of different brain regions, and for 62 the brain as a whole, without the confounds introduced by studying different circuitry in different 63 animals. 64 All data are publicly available through web interfaces. This includes a browser interface, Ne-65 uPrint (Clements et al., 2020), designed so that any interested user can query the hemibrain con-66 nectome even without specific training. NeuPrint can query the connectivity, partners, connection 67 strengths and morphologies of all specified neurons, thus making identifica...

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Section: Supplemental Methodsmentioning

confidence: 99%

A Connectome and Analysis of the AdultDrosophilaCentral Brain

Scheffer

Januszewski

et al. 2020

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162

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“…In parallel to the motion vision pathway of the lobula plate, projection neurons identified in the lobula have been shown to encode moving features such as edges or objects to influence complex vi-sual behaviors (Ache et al, 2019;Aptekar et al, 2015;Frye, 2017a, 2017b;von Reyn et al, 2017;Ribeiro et al, 2018;Wu et al, 2016;Zhang et al, 2013). Roughly 20 classes of lobula columnar neurons (LCs) project to the protocerebrum where axon terminals of each class form tight glomerular neuropils (Otsuna and Ito, 2006;Wu et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Inhibitory Interactions and Columnar Inputs to an Object Motion Detector in Drosophila

et al. 2020

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Graphical Abstract Highlights d LC11 neurons are suppressed by motion and flicker in the local surround d LC11 expresses a GABA receptor required for normal object detection d T2/T3 respond to ON and OFF components of object motion and flicker d T3 neurons excite LC11 and are required for normal LC11 function SUMMARYThe direction-selective T4/T5 cells innervate opticflow processing projection neurons in the lobula plate of the fly that mediate the visual control of locomotion. In the lobula, visual projection neurons coordinate complex behavioral responses to visual features, however, the input circuitry and computations that bestow their feature-detecting properties are less clear. Here, we study a highly specialized small object motion detector, LC11, and demonstrate that its responses are suppressed by local background motion. We show that LC11 expresses GABA-A receptors that serve to sculpt responses to small objects but are not responsible for the rejection of background motion. Instead, LC11 is innervated by columnar T2 and T3 neurons that are themselves highly sensitive to small static or moving objects, insensitive to wide-field motion and, unlike T4/T5, respond to both ON and OFF luminance steps.

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“…Yet, the computations carried out in Drosophila, grasshoppers, and crabs appear very similar at the behavioral level Oliva and Tomsic 2012;von Reyn et al 2014). The biophysics of looming sensitive neurons has long been investigated in grasshoppers and is increasingly well understood in Drosophila (Ache et al 2018;von Reyn et al 2017). Thus, grasshoppers and Drosophila present attractive models to compare and elucidate the relative advantages of harnessing direction-selective and non-direction selective neural circuits for jump escape and how their differences may impact behavior.…”

Section: Discussionmentioning

confidence: 99%

Neuronal ON/OFF Motion Detection Circuits Underlying Looming-Evoked Escape Behavior inDrosophila

Kyung

Dewell

Dierick

et al. 2019

Preprint

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Inactivating fly neurons of the ON or OFF directional motion detection pathways during escape behavior selectively reduced jump responses to light and dark looming stimuli, respectively. AbstractIn Drosophila, early visual processing of motion information segregates in separate ON and OFF pathways. These pathways have been studied in the context of local directional motion detection leading to the encoding of optic flow that provides visual information for flight stabilization. Less is known about their role in detecting impending collision and generating escape behaviors. 'Looming', the simulated approach of an object at constant speed towards an animal, provides a powerful stimulus eliciting jump escape behaviors in stationary flies. We presented looming stimuli mimicking the approach of either a dark object on a bright background or a light object on a dark background, while inactivating neurons belonging either to the ON-or the OFF-motion detection pathways by expressing the dominant Drosophila temperature-sensitive mutant shibire ts in different cells of the ON/OFF pathway. Inactivation of ON, respectively OFF, neurons led to selective decreases in escape behavior to light, resp. dark, looming stimuli. Quantitative analysis showed a nearly perfect splitting of these effects according to the ON/OFF type of the targeted neural populations. Our results suggest that Drosophila ON/OFF motion detection pathways play an important role in controlling jump escape responses according to looming stimulus polarity. They further imply that the biophysical circuits triggering Drosophila jump escape behaviors likely differ substantially from those characterized in other arthropods.

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Neural Basis for Looming Size and Velocity Encoding in the Drosophila Giant Fiber Escape Pathway

Cited by 114 publications

References 52 publications

A Connectome and Analysis of the AdultDrosophilaCentral Brain

A Connectome and Analysis of the AdultDrosophilaCentral Brain

Inhibitory Interactions and Columnar Inputs to an Object Motion Detector in Drosophila

Neuronal ON/OFF Motion Detection Circuits Underlying Looming-Evoked Escape Behavior inDrosophila

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