Axonal gap junctions in the fly visual system enable fast prediction for evasive flight maneuvers

The visual system must make predictions to compensate for inherent delays in its processing, yet little is known, mechanistically, about how prediction aids natural behaviors. Here we show that despite a 30ms intrinsic processing delay, the vertical motion sensitive (VS) network of the blowfly can achieve maximally efficient prediction. This prediction enables fine discrimination of input motion direction during evasive flight maneuvers, which last just 40ms. Combining a rich database of behavioral recordings with detailed compartmental modeling of the VS network, we further show how the VS network implements this optimal prediction. The axonal gap junctions between the VS cells are crucial for optimal prediction during the short timespan of evasive maneuvers. Its subpopulation output further selectively conveys predictive information about the future visual input to the downstream neck motor center. Our work predicts novel sensory-motor pathways that link prediction to behavior.

[1]  Michael H. Dickinson,et al.  Body saccades of Drosophila consist of stereotyped banked turns , 2015, The Journal of Experimental Biology.

[2]  John Guckenheimer,et al.  Discovering the flight autostabilizer of fruit flies by inducing aerial stumbles , 2010, Proceedings of the National Academy of Sciences.

[3]  Michael J. Berry,et al.  Predictive information in a sensory population , 2013, Proceedings of the National Academy of Sciences.

[4]  Alexander A. Alemi,et al.  Deep Variational Information Bottleneck , 2017, ICLR.

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

[6]  M. Dickinson,et al.  Haltere Afferents Provide Direct, Electrotonic Input to a Steering Motor Neuron in the Blowfly, Calliphora , 1996, The Journal of Neuroscience.

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

[8]  Henry Markram,et al.  From Neuron Biophysics to Orientation Selectivity in Electrically Coupled Networks of Neocortical L2/3 Large Basket Cells , 2016, Cerebral cortex.

[9]  Damon A. Clark,et al.  Parallel Computations in Insect and Mammalian Visual Motion Processing , 2016, Current Biology.

[10]  A. Borst,et al.  Neural Action Fields for Optic Flow Based Navigation: A Simulation Study of the Fly Lobula Plate Network , 2011, PloS one.

[11]  N. Strausfeld,et al.  Anatomical organization of retinotopic motion‐sensitive pathways in the optic lobes of flies , 2003, Microscopy research and technique.

[12]  M. Dickinson,et al.  Position‐specific central projections of mechanosensory neurons on the haltere of the blow fly, Calliphora vicina , 1996, The Journal of comparative neurology.

[13]  Hateren,et al.  Blowfly flight and optic flow. II. Head movements during flight , 1999, The Journal of experimental biology.

[14]  W. Buddenbrock Die vermutliche Lösung der Halterenfrage , 1919, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[15]  V. Balasubramanian,et al.  Lag normalization in an electrically coupled neural network , 2013, Nature Neuroscience.

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

[17]  A. Fairhall,et al.  Encoding properties of haltere neurons enable motion feature detection in a biological gyroscope , 2010, Proceedings of the National Academy of Sciences.

[18]  E. Marder Electrical synapses: Beyond speed and synchrony to computation , 1998, Current Biology.

[19]  A Borst,et al.  Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  T. Collett,et al.  Chasing behaviour of houseflies (Fannia canicularis) , 1974, Journal of comparative physiology.

[21]  R. Hengstenberg Mechanosensory control of compensatory head roll during flight in the blowflyCalliphora erythrocephala Meig. , 1988, Journal of Comparative Physiology A.

[22]  Naftali Tishby,et al.  The information bottleneck method , 2000, ArXiv.

[23]  Michael H Dickinson,et al.  The aerodynamics and control of free flight manoeuvres in Drosophila , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  M. Dickinson,et al.  An Integrative Model of Insect Flight Control (Invited) , 2006 .

[25]  J. H. van Hateren,et al.  A theory of maximizing sensory information , 2004, Biological Cybernetics.

[26]  B. Connors Synchrony and so much more: Diverse roles for electrical synapses in neural circuits , 2017, Developmental neurobiology.

[27]  Alexander Borst,et al.  How fly neurons compute the direction of visual motion , 2019, Journal of Comparative Physiology A.

[28]  A. Borst,et al.  Eigenanalysis of a neural network for optic flow processing , 2008 .

[29]  Samuel R. Carroll,et al.  Near-Optimal Decoding of Transient Stimuli from Coupled Neuronal Subpopulations , 2014, The Journal of Neuroscience.

[30]  K. Götz,et al.  Optomotor control of course and altitude in Drosophila melanogaster is correlated with distinct activities of at least three pairs of flight steering muscles. , 1996, The Journal of experimental biology.

[31]  H. López-Schier Neuroplasticity in the acoustic startle reflex in larval zebrafish , 2019, Current Opinion in Neurobiology.

[32]  N. Strausfeld,et al.  The neck motor system of the fly Calliphora erythrocephala. I: Muscles and motor neurons , 1987 .

[33]  M H Dickinson,et al.  Convergent mechanosensory input structures the firing phase of a steering motor neuron in the blowfly, Calliphora. , 1999, Journal of neurophysiology.

[34]  Christopher Burgess,et al.  beta-VAE: Learning Basic Visual Concepts with a Constrained Variational Framework , 2016, ICLR 2016.

[35]  D. Smith,et al.  The fine structure of haltere sensilla in the blowfly Calliphora erythrocephala (Meig.), with scanning electron microscopic observations on the haltere surface. , 1969, Tissue & cell.

[36]  J. Pringle The gyroscopic mechanism of the halteres of Diptera , 1948, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[37]  D. Grimaldi,et al.  Haltere morphology and campaniform sensilla arrangement across Diptera. , 2017, Arthropod structure & development.

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

[39]  K. Catania Tentacled snakes turn C-starts to their advantage and predict future prey behavior , 2009, Proceedings of the National Academy of Sciences.

[40]  W P Chan,et al.  Visual input to the efferent control system of a fly's "gyroscope". , 1998, Science.

[41]  Jonathan P Bacon,et al.  Animal escapology I: theoretical issues and emerging trends in escape trajectories , 2011, Journal of Experimental Biology.

[42]  Alexander Borst,et al.  Reciprocal Inhibitory Connections Within a Neural Network for Rotational Optic-Flow Processing , 2007, Front. Neurosci..

[43]  James E. Fitzgerald,et al.  Nonlinear circuits for naturalistic visual motion estimation , 2015, eLife.

[44]  W. Gronenberg,et al.  Premotor descending neurons responding selectively to local visual stimuli in flies , 1992, The Journal of comparative neurology.

[45]  Joshua W. Shaevitz,et al.  Predictability and hierarchy in Drosophila behavior , 2016, Proceedings of the National Academy of Sciences.

[46]  Michael H Dickinson,et al.  Death Valley, Drosophila, and the Devonian toolkit. , 2014, Annual review of entomology.

[47]  David J Heeger,et al.  Theory of cortical function , 2017, Proceedings of the National Academy of Sciences.

[48]  A. Borst,et al.  Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons , 2004, Nature Neuroscience.

[49]  A. Borst,et al.  Dendro-Dendritic Interactions between Motion-Sensitive Large-Field Neurons in the Fly , 2002, The Journal of Neuroscience.

[50]  K. Götz,et al.  Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster , 1996, Journal of Comparative Physiology A.

[51]  U. Grünert,et al.  Campaniform sensilla of Calliphora vicina (Insecta, Diptera) , 1987, Zoomorphology.

[52]  Richard E. Blahut,et al.  Computation of channel capacity and rate-distortion functions , 1972, IEEE Trans. Inf. Theory.

[53]  Nicholas J. Strausfeld,et al.  Descending pathways connecting the male-specific visual system of flies to the neck and flight motor , 1991, Journal of Comparative Physiology A.

[54]  Olivier Marre,et al.  Relevant sparse codes with variational information bottleneck , 2016, NIPS.

[55]  N. Strausfeld,et al.  The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica , 1985, Cell and Tissue Research.

[56]  Z. J. Wang,et al.  Fruit flies modulate passive wing pitching to generate in-flight turns. , 2009, Physical review letters.

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

[58]  Hateren,et al.  Blowfly flight and optic flow. I. Thorax kinematics and flight dynamics , 1999, The Journal of experimental biology.

[59]  Cheng Lyu,et al.  Quantitative Predictions Orchestrate Visual Signaling in Drosophila , 2017, Cell.

[60]  Alexander Borst,et al.  Preserving Neural Function under Extreme Scaling , 2013, PloS one.

[61]  Michael H Dickinson,et al.  The visual control of landing and obstacle avoidance in the fruit fly Drosophila melanogaster , 2012, Journal of Experimental Biology.

[62]  Alexander Borst,et al.  Local motion detectors are required for the computation of expansion flow-fields , 2015, Biology Open.

[63]  Michael H. Dickinson,et al.  Flies Evade Looming Targets by Executing Rapid Visually Directed Banked Turns , 2014, Science.

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

[65]  Idan Segev,et al.  Robust coding of flow-field parameters by axo-axonal gap junctions between fly visual interneurons , 2007, Proceedings of the National Academy of Sciences.

[66]  Stephanie E Palmer,et al.  Learning to make external sensory stimulus predictions using internal correlations in populations of neurons , 2017, Proceedings of the National Academy of Sciences.

[67]  A. Borst Fly visual course control: behaviour, algorithms and circuits , 2014, Nature Reviews Neuroscience.

[68]  M. Dickinson,et al.  Summation of visual and mechanosensory feedback in Drosophila flight control , 2004, Journal of Experimental Biology.

[69]  Idan Segev,et al.  Optimization principles of dendritic structure , 2007, Theoretical Biology and Medical Modelling.

[70]  N. Strausfeld,et al.  The relevance of neural architecture to visual performance: Phylogenetic conservation and variation in dipteran visual systems , 1997 .

[71]  R. Chevalier The fine structure of campaniform sensilla on the halteres of Drosophila melanogaster , 1969 .

[72]  A. Borst,et al.  Robust Coding of Ego-Motion in Descending Neurons of the Fly , 2009, The Journal of Neuroscience.

[73]  Greg Wayne,et al.  A temporal basis for predicting the sensory consequences of motor commands in an electric fish , 2014, Nature Neuroscience.

[74]  Alexander Borst,et al.  Different receptive fields in axons and dendrites underlie robust coding in motion-sensitive neurons , 2009, Nature Neuroscience.

[75]  Michael H. Dickinson,et al.  Flies Regulate Wing Motion via Active Control of a Dual-Function Gyroscope , 2019, Current Biology.

[76]  M. S. Tu,et al.  The control of wing kinematics by two steering muscles of the blowfly (Calliphora vicina) , 1996, Journal of Comparative Physiology A.

[77]  M. Dickinson,et al.  A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster , 2003, Journal of Experimental Biology.

[78]  Y. Toh Structure of campaniform sensilla on the haltere ofDrosophila prepared by cryofixation , 1985 .

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

[80]  E.J. Chichilnisky,et al.  Cone photoreceptor contributions to noise and correlations in the retinal output , 2011, Nature Neuroscience.

[81]  Zachary F. Jessen,et al.  A Self-Regulating Gap Junction Network of Amacrine Cells Controls Nitric Oxide Release in the Retina , 2018, Neuron.

[82]  N. J. Strausfeld,et al.  Convergence of visual, haltere, and prosternai inputs at neck motor neurons of Calliphora erythrocephala , 1985, Cell and Tissue Research.

[83]  M. Dickinson,et al.  The correlation between wing kinematics and steering muscle activity in the blowfly Calliphora vicina. , 2001, The Journal of experimental biology.

[84]  Alexander Borst,et al.  Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly , 2005, Journal of Comparative Physiology A.

[85]  A. Kraskov,et al.  Estimating mutual information. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[86]  Alexander Borst,et al.  The intrinsic electrophysiological characteristics of fly lobula plate tangential cells: I. Passive membrane properties , 1996, Journal of Computational Neuroscience.

[87]  Siwei Wang,et al.  Efficient encoding of motion is mediated by gap junctions in the fly visual system , 2017, PLoS Comput. Biol..

[88]  Alexander Borst,et al.  Integration of Lobula Plate Output Signals by DNOVS1, an Identified Premotor Descending Neuron , 2007, The Journal of Neuroscience.

[89]  M. Dickinson,et al.  Visually Mediated Motor Planning in the Escape Response of Drosophila , 2008, Current Biology.

[90]  Michael Dickinson,et al.  The Function and Organization of the Motor System Controlling Flight Maneuvers in Flies , 2017, Current Biology.

[91]  Samuel T Fabian,et al.  Interception by two predatory fly species is explained by a proportional navigation feedback controller , 2018, Journal of The Royal Society Interface.