Parallel encoding of recent visual experience and self-motion during navigation in Drosophila

Animal navigation requires multiple types of information for decisions on directional heading. We identified neural processing channels that encode multiple cues during navigational decision-making in Drosophila melanogaster. In a flight simulator, we found that flies made directional choices on the basis of the location of a recently presented landmark. This experience-guided navigation was impaired by silencing neurons in the bulb (BU), a region in the central brain. Two-photon calcium imaging during flight revealed that the dorsal part of the BU encodes the location of a recent landmark, whereas the ventral part of the BU tracks self-motion reflecting turns. Photolabeling-based circuit tracing indicated that these functional compartments of the BU constitute adjacent, yet distinct, anatomical pathways that both enter the navigation center. Thus, the fly's navigation system organizes multiple types of information in parallel channels, which may compactly transmit signals without interference for decision-making during flight.

[1]  Michael H. Dickinson,et al.  A modular display system for insect behavioral neuroscience , 2008, Journal of Neuroscience Methods.

[2]  M. Heisenberg,et al.  Vision in Drosophila , 1984 .

[3]  Anmo J Kim,et al.  Cellular evidence for efference copy in Drosophila visuomotor processing , 2015, Nature Neuroscience.

[4]  Michael H. Dickinson,et al.  Olfactory modulation of flight in Drosophila is sensitive, selective and rapid , 2010, Journal of Experimental Biology.

[5]  Gerald M Rubin,et al.  Using translational enhancers to increase transgene expression in Drosophila , 2012, Proceedings of the National Academy of Sciences.

[6]  P. Dudchenko An overview of the tasks used to test working memory in rodents , 2004, Neuroscience & Biobehavioral Reviews.

[7]  G. Davis,et al.  Homeostatic Control of Presynaptic Release Is Triggered by Postsynaptic Membrane Depolarization , 2001, Neuron.

[8]  Michael H. Dickinson,et al.  A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila , 2017, Current Biology.

[9]  G. Rubin,et al.  Refinement of Tools for Targeted Gene Expression in Drosophila , 2010, Genetics.

[10]  T. Collett,et al.  Animal Navigation: Path Integration, Visual Landmarks and Cognitive Maps , 2004, Current Biology.

[11]  Karl Georg Götz,et al.  Optomotor control of wing beat and body posture in drosophila , 1979, Biological Cybernetics.

[12]  J. Armstrong,et al.  Structure of the adult central complex in Drosophila: Organization of distinct neuronal subsets , 2010, The Journal of comparative neurology.

[13]  N. Strausfeld,et al.  Subdivision of the drosophila mushroom bodies by enhancer-trap expression patterns , 1995, Neuron.

[14]  R. Strauss,et al.  Visual Working Memory Requires Permissive and Instructive NO/cGMP Signaling at Presynapses in the Drosophila Central Brain , 2017, Current Biology.

[15]  Hanchuan Peng,et al.  Clonal Development and Organization of the Adult Drosophila Central Brain , 2013, Current Biology.

[16]  M. Heisenberg,et al.  Neuronal architecture of the central complex in Drosophila melanogaster , 2004, Cell and Tissue Research.

[17]  R. Strauss,et al.  Analysis of a spatial orientation memory in Drosophila , 2008, Nature.

[18]  M Heisenberg,et al.  Visual pattern memory without shape recognition. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[19]  Hokto Kazama,et al.  Decoding of Context-Dependent Olfactory Behavior in Drosophila , 2016, Neuron.

[20]  Michael H Dickinson,et al.  Visual stimulation of saccades in magnetically tethered Drosophila , 2006, Journal of Experimental Biology.

[21]  Aljoscha Nern,et al.  Neural signatures of dynamic stimulus selection in Drosophila , 2017, Nature Neuroscience.

[22]  J. Armstrong,et al.  Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. , 1999, Journal of neurobiology.

[23]  Matthew Collett,et al.  Path integration in insects , 2000, Current Opinion in Neurobiology.

[24]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[25]  Vivek Jayaraman,et al.  The insect central complex , 2016, Current Biology.

[26]  V. Jayaraman,et al.  Ring attractor dynamics in the Drosophila central brain , 2017, Science.

[27]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[28]  Meixia Li,et al.  A conditioned visual orientation requires the ellipsoid body in Drosophila , 2015, Learning & memory.

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

[30]  Michael H Dickinson,et al.  Spatial organization of visuomotor reflexes in Drosophila , 2004, Journal of Experimental Biology.

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

[32]  Barry J. Dickson,et al.  The Drosophila pheromone cVA activates a sexually dimorphic neural circuit , 2008, Nature.

[33]  K. Götz Course-control, metabolism and wing interference during ultralong tethered flight in Drosophila melanogaster , 1987 .

[34]  M. Heisenberg,et al.  Attracting the attention of a fly , 2011, Proceedings of the National Academy of Sciences.

[35]  Peter T Weir,et al.  Functional divisions for visual processing in the central brain of flying Drosophila , 2015, Proceedings of the National Academy of Sciences.

[36]  Kei Ito,et al.  Systematic Analysis of Neural Projections Reveals Clonal Composition of the Drosophila Brain , 2013, Current Biology.

[37]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Michael H Dickinson,et al.  The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. , 2002, The Journal of experimental biology.

[39]  M. Quirk,et al.  Representation of Spatial Goals in Rat Orbitofrontal Cortex , 2006, Neuron.

[40]  Charalambos P. Kyriacou,et al.  Unexpected features of Drosophila circadian behavioural rhythms under natural conditions , 2012, Nature.

[41]  R. Wolf,et al.  Reafferent control of optomotor yaw torque inDrosophila melanogaster , 1988, Journal of Comparative Physiology A.

[42]  Michael H. Dickinson,et al.  Motmot, an open-source toolkit for realtime video acquisition and analysis , 2009, Source Code for Biology and Medicine.

[43]  M. Dickinson,et al.  Active flight increases the gain of visual motion processing in Drosophila , 2010, Nature Neuroscience.

[44]  Jamey S. Kain,et al.  Neuronal control of locomotor handedness in Drosophila , 2014 .

[45]  Michael B. Reiser,et al.  Two-photon calcium imaging from motion-sensitive neurons in head-fixed Drosophila during optomotor walking behavior , 2010, Nature Methods.

[46]  Johannes D. Seelig,et al.  Feature detection and orientation tuning in the Drosophila central complex , 2013, Nature.

[47]  Volker Hartenstein,et al.  Visual Input to the Drosophila Central Complex by Developmentally and Functionally Distinct Neuronal Populations , 2017, Current Biology.

[48]  R. Ritzmann,et al.  Central-Complex Control of Movement in the Freely Walking Cockroach , 2015, Current Biology.

[49]  Thomas S. Collett,et al.  Memory use in insect visual navigation , 2002, Nature Reviews Neuroscience.

[50]  Johannes D. Seelig,et al.  Angular velocity integration in a fly heading circuit , 2017, eLife.

[51]  George H. Patterson,et al.  A Photoactivatable GFP for Selective Photolabeling of Proteins and Cells , 2002, Science.

[52]  Gaby Maimon,et al.  A neural circuit architecture for angular integration in Drosophila , 2017, Nature.

[53]  Michael B. Reiser,et al.  Visual Place Learning in Drosophila melanogaster , 2011, Nature.

[54]  Richard Axel,et al.  A dimorphic pheromone circuit in Drosophila from sensory input to descending output , 2010, Nature.

[55]  G. Rubin,et al.  Neuroarchitecture and neuroanatomy of the Drosophila central complex: A GAL4-based dissection of protocerebral bridge neurons and circuits , 2014, The Journal of comparative neurology.

[56]  Michael H. Dickinson,et al.  Cellular mechanisms for integral feedback in visually guided behavior , 2014, Proceedings of the National Academy of Sciences.

[57]  Michael H. Dickinson,et al.  A Simple Vision-Based Algorithm for Decision Making in Flying Drosophila , 2008, Current Biology.

[58]  Roland Strauss,et al.  The visual orientation memory of Drosophila requires Foraging (PKG) upstream of Ignorant (RSK2) in ring neurons of the central complex. , 2012, Learning & memory.

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

[60]  Stefano Fusi,et al.  Hippocampal-prefrontal input supports spatial encoding in working memory , 2015, Nature.

[61]  J. Taube The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.

[62]  M. Tsodyks,et al.  Working models of working memory , 2014, Current Opinion in Neurobiology.

[63]  Reinhard Wolf,et al.  Central complex and mushroom bodies mediate novelty choice behavior in Drosophila , 2015, Journal of neurogenetics.

[64]  Edvard I. Moser,et al.  Speed cells in the medial entorhinal cortex , 2015, Nature.

[65]  Volker Hartenstein,et al.  Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones. , 2013, Developmental biology.

[66]  Johannes D. Seelig,et al.  Neural dynamics for landmark orientation and angular path integration , 2015, Nature.

[67]  J. Kennedy Zigzagging and casting as a programmed response to wind‐borne odour: a review , 1983 .

[68]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[69]  U. Homberg,et al.  Organization and functional roles of the central complex in the insect brain. , 2014, Annual review of entomology.

[70]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[71]  M. Heisenberg,et al.  Visual Attention in Flies—Dopamine in the Mushroom Bodies Mediates the After-Effect of Cueing , 2016, PloS one.

[72]  Marta Coelho Antunes,et al.  The novel object recognition memory: neurobiology, test procedure, and its modifications , 2011, Cognitive Processing.

[73]  M. Heisenberg,et al.  Vision in Flies: Measuring the Attention Span , 2016, PloS one.