Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain

Understanding the circuit mechanisms behind motion detection is a long-standing question in visual neuroscience. In Drosophila melanogaster, recently discovered synapse-level connectomes in the optic lobe, particularly in ON-pathway (T4) receptive-field circuits, in concert with physiological studies, suggest a motion model that is increasingly intricate when compared with the ubiquitous Hassenstein-Reichardt model. By contrast, our knowledge of OFF-pathway (T5) has been incomplete. Here, we present a conclusive and comprehensive connectome that, for the first time, integrates detailed connectivity information for inputs to both the T4 and T5 pathways in a single EM dataset covering the entire optic lobe. With novel reconstruction methods using automated synapse prediction suited to such a large connectome, we successfully corroborate previous findings in the T4 pathway and comprehensively identify inputs and receptive fields for T5. Although the two pathways are probably evolutionarily linked and exhibit many similarities, we uncover interesting differences and interactions that may underlie their distinct functional properties.

[1]  Alexander Borst,et al.  A biophysical mechanism for preferred direction enhancement in fly motion vision , 2018, PLoS Comput. Biol..

[2]  I. Meinertzhagen Of what use is connectomics? A personal perspective on the Drosophila connectome , 2018, Journal of Experimental Biology.

[3]  C. Desplan,et al.  Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit , 2018, Cell.

[4]  Michael B. Reiser,et al.  Simple integration of fast excitation and offset, delayed inhibition computes directional selectivity in Drosophila , 2017, Nature Neuroscience.

[5]  Michael B. Reiser,et al.  Ultra-selective looming detection from radial motion opponency , 2017, Nature.

[6]  Barry J. Dickson,et al.  The VT GAL4, LexA, and split-GAL4 driver line collections for targeted expression in the Drosophila nervous system , 2017, bioRxiv.

[7]  G. Rubin,et al.  Genetic Reagents for Making Split-GAL4 Lines in Drosophila , 2017, Genetics.

[8]  A. Borst,et al.  A common directional tuning mechanism of Drosophila motion-sensing neurons in the ON and in the OFF pathway , 2017, eLife.

[9]  K. Hayworth,et al.  Enhanced FIB-SEM systems for large-volume 3D imaging , 2017, eLife.

[10]  Aljoscha Nern,et al.  The comprehensive connectome of a neural substrate for ‘ON’ motion detection in Drosophila , 2017, eLife.

[11]  A. Borst,et al.  Transgenic line for the identification of cholinergic release sites in Drosophila melanogaster , 2017, Journal of Experimental Biology.

[12]  Michael B. Reiser,et al.  The Emergence of Directional Selectivity in the Visual Motion Pathway of Drosophila , 2017, Neuron.

[13]  Michael S. Drews,et al.  The Temporal Tuning of the Drosophila Motion Detectors Is Determined by the Dynamics of Their Input Elements , 2017, Current Biology.

[14]  Fred A Hamprecht,et al.  Multicut brings automated neurite segmentation closer to human performance , 2017, Nature Methods.

[15]  Matthew S. Creamer,et al.  Direct Measurement of Correlation Responses in Drosophila Elementary Motion Detectors Reveals Fast Timescale Tuning , 2016, Neuron.

[16]  Alexander Borst,et al.  Complementary mechanisms create direction selectivity in the fly , 2016, eLife.

[17]  Ben Poole,et al.  Direction Selectivity in Drosophila Emerges from Preferred-Direction Enhancement and Null-Direction Suppression , 2016, The Journal of Neuroscience.

[18]  I. Salecker,et al.  Retinal determination genes coordinate neuroepithelial specification and neurogenesis modes in the Drosophila optic lobe , 2016, Development.

[19]  Louis K. Scheffer,et al.  Fully-Automatic Synapse Prediction and Validation on a Large Data Set , 2016, Front. Neural Circuits.

[20]  I. Meinertzhagen Connectome studies on Drosophila: a short perspective on a tiny brain , 2016, Journal of neurogenetics.

[21]  Stephen M. Plaza,et al.  Large-Scale Electron Microscopy Image Segmentation in Spark , 2016, ArXiv.

[22]  A. Borst,et al.  Comprehensive Characterization of the Major Presynaptic Elements to the Drosophila OFF Motion Detector , 2016, Neuron.

[23]  Thomas R. Clandinin,et al.  A Class of Visual Neurons with Wide-Field Properties Is Required for Local Motion Detection , 2015, Current Biology.

[24]  Louis K. Scheffer,et al.  Synaptic circuits and their variations within different columns in the visual system of Drosophila , 2015, Proceedings of the National Academy of Sciences.

[25]  Alexander Borst,et al.  Neural Circuit to Integrate Opposing Motions in the Visual Field , 2015, Cell.

[26]  Ian A. Meinertzhagen,et al.  A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system , 2015, Front. Neural Circuits.

[27]  A. Borst,et al.  Common circuit design in fly and mammalian motion vision , 2015, Nature Neuroscience.

[28]  Aljoscha Nern,et al.  Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system , 2015, Proceedings of the National Academy of Sciences.

[29]  Jinhyun Kim,et al.  neuTube 1.0: A New Design for Efficient Neuron Reconstruction Software Based on the SWC Format 123 , 2015, eNeuro.

[30]  Alexander Borst,et al.  In search of the holy grail of fly motion vision , 2014, The European journal of neuroscience.

[31]  Damon A. Clark,et al.  Processing properties of ON and OFF pathways for Drosophila motion detection , 2014, Nature.

[32]  Anirban Chakraborty,et al.  A Context-Aware Delayed Agglomeration Framework for Electron Microscopy Segmentation , 2014, PloS one.

[33]  Ian A. Meinertzhagen,et al.  Candidate Neural Substrates for Off-Edge Motion Detection in Drosophila , 2014, Current Biology.

[34]  Bassem A. Hassan,et al.  Proper connectivity of Drosophila motion detector neurons requires Atonal function in progenitor cells , 2014, Neural Development.

[35]  A. Borst,et al.  Neural Circuit Components of the Drosophila OFF Motion Vision Pathway , 2014, Current Biology.

[36]  G. Rubin,et al.  A directional tuning map of Drosophila elementary motion detectors , 2013, Nature.

[37]  Louis K. Scheffer,et al.  A visual motion detection circuit suggested by Drosophila connectomics , 2013, Nature.

[38]  D. Pisani,et al.  Molecular Timetrees Reveal a Cambrian Colonization of Land and a New Scenario for Ecdysozoan Evolution , 2013, Current Biology.

[39]  Julie H. Simpson,et al.  A GAL4-driver line resource for Drosophila neurobiology. , 2012, Cell reports.

[40]  Ian A. Meinertzhagen,et al.  Wiring Economy and Volume Exclusion Determine Neuronal Placement in the Drosophila Brain , 2011, Current Biology.

[41]  Ullrich Köthe,et al.  Ilastik: Interactive learning and segmentation toolkit , 2011, 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[42]  Kei Ito,et al.  Concentric zones, cell migration and neuronal circuits in the Drosophila visual center , 2011, Neuroscience Research.

[43]  Alexander Borst,et al.  ON and OFF pathways in Drosophila motion vision , 2010, Nature.

[44]  Hanchuan Peng,et al.  V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets , 2010, Nature Biotechnology.

[45]  Shin-ya Takemura,et al.  Synaptic circuits of the Drosophila optic lobe: The input terminals to the medulla , 2008, The Journal of comparative neurology.

[46]  Ian A. Meinertzhagen,et al.  Glutamate, GABA and Acetylcholine Signaling Components in the Lamina of the Drosophila Visual System , 2008, PloS one.

[47]  G. Knott,et al.  Serial Section Scanning Electron Microscopy of Adult Brain Tissue Using Focused Ion Beam Milling , 2008, The Journal of Neuroscience.

[48]  Kei Ito,et al.  Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula‐specific pathways , 2006, The Journal of comparative neurology.

[49]  Stephan J. Sigrist,et al.  Bruchpilot, a Protein with Homology to ELKS/CAST, Is Required for Structural Integrity and Function of Synaptic Active Zones in Drosophila , 2006, Neuron.

[50]  Tobias M. Rasse,et al.  Bruchpilot, a Protein with Homology to ELKS/CAST, Is Required for Structural Integrity and Function of Synaptic Active Zones in Drosophila , 2006, Neuron.

[51]  N. Strausfeld,et al.  Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa , 2003, The Journal of comparative neurology.

[52]  Liqun Luo,et al.  Structure of the vertical and horizontal system neurons of the lobula plate in Drosophila , 2002, The Journal of comparative neurology.

[53]  N. Strausfeld,et al.  Visual Motion-Detection Circuits in Flies: Small-Field Retinotopic Elements Responding to Motion Are Evolutionarily Conserved across Taxa , 1996, The Journal of Neuroscience.

[54]  I. Meinertzhagen,et al.  Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster , 1991, The Journal of comparative neurology.

[55]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure , 1989, Cell and Tissue Research.

[56]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[57]  B. Hassenstein,et al.  Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus , 1956 .

[58]  D. Tomsic,et al.  A crustacean lobula plate: Morphology, connections, and retinotopic organization , 2018, The Journal of comparative neurology.

[59]  B. Heming BOOK REVIEW: Strausfeld N.J. 2012: ARTHROPOD BRAINS. EVOLUTION, FUNCTIONAL ELEGANCE, AND HISTORICAL SIGNIFICANCE. , 2013 .

[60]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster , 2004, Cell and Tissue Research.

[61]  I. Meinertzhagen,et al.  Synaptic organization in the fly's optic lamina: few cells, many synapses and divergent microcircuits. , 2001, Progress in brain research.

[62]  Santiago Ramón y Cajal,et al.  Contribución al conocimiento de los centros nerviosos de los insectos / por S.R. Cajal y D. Sánchez. , 1915 .

[63]  R. Cooper Sensory Communication , 2022 .