Neural Circuit to Integrate Opposing Motions in the Visual Field

When navigating in their environment, animals use visual motion cues as feedback signals that are elicited by their own motion. Such signals are provided by wide-field neurons sampling motion directions at multiple image points as the animal maneuvers. Each one of these neurons responds selectively to a specific optic flow-field representing the spatial distribution of motion vectors on the retina. Here, we describe the discovery of a group of local, inhibitory interneurons in the fruit fly Drosophila key for filtering these cues. Using anatomy, molecular characterization, activity manipulation, and physiological recordings, we demonstrate that these interneurons convey direction-selective inhibition to wide-field neurons with opposite preferred direction and provide evidence for how their connectivity enables the computation required for integrating opposing motions. Our results indicate that, rather than sharpening directional selectivity per se, these circuit elements reduce noise by eliminating non-specific responses to complex visual information.

[1]  N. Strausfeld,et al.  Dissection of the Peripheral Motion Channel in the Visual System of Drosophila melanogaster , 2007, Neuron.

[2]  K. Hausen Functional Characterization and Anatomical Identification of Motion Sensitive Neurons in the Lobula plate of the Blowfly Calliphora erythrocephala , 1976 .

[3]  Alexander Borst,et al.  Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila , 2010, Nature Neuroscience.

[4]  W. Reichardt,et al.  Computational structure of a biological motion-detection system as revealed by local detector analysis in the fly's nervous system. , 1989, Journal of the Optical Society of America. A, Optics and image science.

[5]  An intracellular recording study of stimulus-specific response properties in cat area 17 , 1991, Brain Research.

[6]  Hammad Qureshi Contributions , 1974, Livre Blanc de la Recherche en Mécanique.

[7]  T. Collett,et al.  Binocular, Directionally Selective Neurones, Possibly Involved in the Optomotor Response of Insects , 1966, Nature.

[8]  Y. Diao,et al.  Sensitivity of LS neurons to optic flow stimuli , 1997 .

[9]  Michael R. Ibbotson,et al.  Wide-field motion-sensitive neurons tuned to horizontal movement in the honeybee, Apis mellifera , 2004, Journal of Comparative Physiology A.

[10]  Ian A. Meinertzhagen,et al.  Cholinergic Circuits Integrate Neighboring Visual Signals in a Drosophila Motion Detection Pathway , 2011, Current Biology.

[11]  A. Borst,et al.  Subcellular mapping of dendritic activity in optic flow processing neurons , 2014, Journal of Comparative Physiology A.

[12]  A. Borst,et al.  Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila , 2012, Journal of Comparative Physiology.

[13]  J. van Santen,et al.  Elaborated Reichardt detectors. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[14]  K. Fischbach,et al.  Activity labeling patterns in the medulla of Drosophila melanogaster caused by motion stimuli , 1992, Cell and Tissue Research.

[15]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[16]  B Schnell,et al.  Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. , 2010, Journal of neurophysiology.

[17]  P. Detwiler,et al.  Directionally selective calcium signals in dendrites of starburst amacrine cells , 2002, Nature.

[18]  A. Borst,et al.  Internal Structure of the Fly Elementary Motion Detector , 2011, Neuron.

[19]  Edward M. Callaway,et al.  A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex , 2014 .

[20]  C. W. Oyster,et al.  Information processing in the rabbit visual system , 1971, Documenta Ophthalmologica.

[21]  A. Borst,et al.  Cholinergic and GABAergic receptors on fly tangential cells and their role in visual motion detection. , 1996, Journal of neurophysiology.

[22]  Srinivas C. Turaga,et al.  Space-time wiring specificity supports direction selectivity in the retina , 2014, Nature.

[23]  Jasper Akerboom,et al.  Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging , 2012, The Journal of Neuroscience.

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

[25]  Cori Bargmann,et al.  GFP Reconstitution Across Synaptic Partners (GRASP) Defines Cell Contacts and Synapses in Living Nervous Systems , 2008, Neuron.

[26]  Mark A. Frye,et al.  Olfactory Neuromodulation of Motion Vision Circuitry in Drosophila , 2015, Current Biology.

[27]  K. Hausen,et al.  The synaptic organization of visual interneurons in the lobula complex of flies , 1980, Cell and Tissue Research.

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

[29]  Alexander Borst,et al.  Mechanisms of dendritic integration underlying gain control in fly motion-sensitive interneurons , 1995, Journal of Computational Neuroscience.

[30]  M. Schnitzer,et al.  GABAergic Lateral Interactions Tune the Early Stages of Visual Processing in Drosophila , 2013, Neuron.

[31]  A. Borst,et al.  Response Properties of Motion-Sensitive Visual Interneurons in the Lobula Plate of Drosophila melanogaster , 2008, Current Biology.

[32]  Alexander Borst,et al.  The role of GABA in detecting visual motion , 1990, Brain Research.

[33]  Alexander Borst,et al.  Object tracking in motion-blind flies , 2013, Nature Neuroscience.

[34]  Ian Nauhaus,et al.  Anterior-Posterior Direction Opponency in the Superficial Mouse Lateral Geniculate Nucleus , 2012, Neuron.

[35]  Alexander Borst,et al.  Nonlinear Integration of Binocular Optic Flow by DNOVS2, A Descending Neuron of the Fly , 2008, The Journal of Neuroscience.

[36]  A. Borst,et al.  Dendritic Computation of Direction Selectivity and Gain Control in Visual Interneurons , 1997, The Journal of Neuroscience.

[37]  C. W. Oyster,et al.  Rabbit Lateral Geniculate Nucleus: Sharpener of Directional Information , 1969, Science.

[38]  K. Hausen The Lobula-Complex of the Fly: Structure, Function and Significance in Visual Behaviour , 1984 .

[39]  Konrad Basler,et al.  Organizing activity of wingless protein in Drosophila , 1993, Cell.

[40]  Andrew D Huberman,et al.  Diverse Visual Features Encoded in Mouse Lateral Geniculate Nucleus , 2013, The Journal of Neuroscience.

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

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

[43]  K. Broadie,et al.  Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects , 1995, Neuron.

[44]  Charles L. Cox,et al.  Glutamate locally activates dendritic outputs of thalamic interneurons , 1998, Nature.

[45]  Chuan Yi Tang,et al.  A 2.|E|-Bit Distributed Algorithm for the Directed Euler Trail Problem , 1993, Inf. Process. Lett..

[46]  A. Borst,et al.  Fly motion vision. , 2010, Annual review of neuroscience.

[47]  A. Borst,et al.  Direction selectivity of blowfly motion-sensitive neurons is computed in a two-stage process. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Damon A. Clark,et al.  Defining the Computational Structure of the Motion Detector in Drosophila , 2011, Neuron.

[49]  Werner Reichardt,et al.  Evaluation of optical motion information by movement detectors , 1987, Journal of Comparative Physiology A.

[50]  Rachel I. Wilson,et al.  Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system , 2013, Proceedings of the National Academy of Sciences.

[51]  Alexander Borst,et al.  Optogenetic and Pharmacologic Dissection of Feedforward Inhibition in Drosophila Motion Vision , 2014, The Journal of Neuroscience.

[52]  Alexander Borst,et al.  Functional Specialization of Parallel Motion Detection Circuits in the Fly , 2013, The Journal of Neuroscience.

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

[54]  E. Marder,et al.  The pharmacological properties of some crustacean neuronal acetylcholine, gamma‐aminobutyric acid, and L‐glutamate responses. , 1978, The Journal of physiology.

[55]  W Singer,et al.  Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. , 1977, Physiological reviews.

[56]  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.

[57]  Damon A. Clark,et al.  Modular Use of Peripheral Input Channels Tunes Motion-Detecting Circuitry , 2013, Neuron.

[58]  B. Frost,et al.  Common reference frame for neural coding of translational and rotational optic flow , 1998, Nature.

[59]  G. Rubin,et al.  Tools for neuroanatomy and neurogenetics in Drosophila , 2008, Proceedings of the National Academy of Sciences.

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

[61]  W. Denk,et al.  Two-photon laser scanning fluorescence microscopy. , 1990, Science.

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

[63]  Michael B. Reiser,et al.  Contributions of the 12 Neuron Classes in the Fly Lamina to Motion Vision , 2013, Neuron.

[64]  Xin Wang,et al.  Thalamic interneurons and relay cells use complementary synaptic mechanisms for visual processing , 2010, Nature Neuroscience.

[65]  R. Hengstenberg,et al.  Estimation of self-motion by optic flow processing in single visual interneurons , 1996, Nature.