How Do Ants Navigate in Natural Environments?
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How do ants navigate in natural environments? Antoine Wystrach Learning walks scan scan scan scan scan Mueller and Wehner 2010 Curr biol Path Integration Fleishmann et al., 2018 Curr biol scan scan scan scan scan Mueller and Wehner 2010 Curr biol Path Integration Food item Ophion obscuratus. Credit: Matthias Lenke/Flickr.co Path Integration Food item Path Integration Food item Wehner 2003. J Comp Physiol A Path - Accumulate errors Integration Food item - Accumulate errors Path - Passive displacement Integration Food item Wehner and Srinivasan 1981. J. comp. phys Path Systematic Integration Search Food item Wehner and Räber 1979. Experencia Cartwright and Collett 1983. J. comp. phys Path Visual scene Systematic Integration navigation Search Food item Wehner and Räber 1979. Experencia Cartwright and Collett 1983. J. comp. phys Path Visual scene Systematic Integration navigation Search Food item Path Visual scene Systematic Integration navigation Search Wehner 2008. Myrmec. news Path Visual scene Systematic navigation Integration Search Wehner 2008. Myrmec. news Gigantiops destructor Gigantiops destructor Path Visual scene Systematic Integration navigation Search Beugnon et al., 2005. J. insect behav. Gigantiops destructor Gigantiops destructor Kohler and Wehner 2005. Neurobiol. Learn. Mem. Melophorus bagoti Route following Kohler and Wehner 2005. Neurobiol. Learn. Mem. Melophorus bagoti Melophorus bagoti Route following Kohler and Wehner 2005. Neurobiol. Learn. Mem. Melophorus bagoti Landmarks ? Melophorus bagoti Nest Wystrach et al. 2011. JCPA Nest Wystrach et al. 2011. JCPA Melophorus bagoti Landmarks or panorama ? Melophorus bagoti Wystrach et al., 2011. Front. In Zool. Ant paths Quantifying visual Information Ant eye 1 pixel / 4 deg Wystrach et al., 2011. Front. In Zool. Human resolution Ant resolution Ant paths Picture based Hypotheses predictions Wystrach et al., 2011. Front. In Zool. Ant paths Picture based Hypotheses predictions Wystrach et al., 2011. Front. In Zool. Cataglyphis velox Ant tracking in the field HABITRACKS Risse et al., (submited to Nature Methods) Accurate tracking in the field Ant tracking in the field HABITRACKS Risse et al., (submited to Nature Methods) Accurate tracking in the field Ant tracking in the field HABITRACKS HABITAT-3D Accurate reconstruction of natural habitats Ant tracking in the field HABITRACKS HABITAT-3D ANT EYE MODEL Reconstruction of ants’ visuo-motor experience Show the movie Motor pattern observation Real ant route Ants’ paths are oscillating Lent et al., 2013 Proc. Roy. Soc. B A simple oscillator model oscillator Real ant route View familiarity modulate the oscillator Kodzhabashev et al., 2015 Biomim. Syst. A simple oscillator model oscillator Real ant route View familiarity modulate the oscillator Kodzhabashev et al., 2015 Biomim. Syst. A simple oscillator model Tested on 15 ants’ route Mean: 1 error/12.8m travelled Oscillator model Real ant route Kodzhabashev et al., 2015 Biomim. Syst. A simple oscillator model Oscillator model Real ant route To explore emerging proprieties When lost, scanning behaviour emerges! Kodzhabashev et al., 2015 Biomim. Syst. Ants vs. Model prediction Ants scan when lost Real ant route Wystrach et al., (2014) Ants vs. Model prediction Real ant route Mangan et al. 2012, Behav. Ecol Wystrach et al., (2014) Ants vs. Model prediction Learning walks For a naïve ant, the world looks unfamiliar scan scan scan scan scan Mueller and Wehner 2010 Curr biol Ants vs. Model prediction Real ant route mismatch Visual Visual Displacement (m) Wystrach et al. 2011. JCPA Neural implementation ? oscillator The connectome !! Eichler et al. "Nature 548.7666 (2017): 175. Aso, Y (2014) Elife, 3, e04577. Risse et al., 2013 Plos One Chemotaxis in larva Gomez-Marin et al., 2011. Nat. com Chemotaxis in larva Gomez-Marin et al., 2011. Nat. com Wystrach et al., 2016 Elife Simulation of larva chemotaxis Wystrach et al., 2016 Elife Simulation of larva chemotaxis Wystrach et al., 2016 Elife Larvae vs. Model predictions Wystrach et al., 2016 Elife Larvae vs. Model predictions Wystrach et al., 2016 Elife Learning assays Schleyer et al., 2011 Learn. & Mem Learning assays Asso centre ∑ Schleyer et al., 2011 Learn. & Mem The Mushroom bodies: an associative centre Heisenberg 2003 Nature Rev. Neurosc. Aso et al., 2016 Elife Simple summation of signals Asso centre ∑ Appetitive learning Aversive learning Innate Wystrach et al., 2016 Elife ∑ Motor effect of learning Motor effect of sugar Across sensory modalities Across sensory modalities Bellman et al., 2010; Front. in Neurosci. Across sensory modalities Flexibility for modulation/innovation. Across species? Route Following Plume Tracking Homing Mangan and Webb 2012 Taxis Pansopha, Ando and Kanzaki. 2014 Gomez-Marin et al., 2011 Philippides et al., 2013 Olfactory input into the mushroom body oscillator Heisenberg 2003 Nature Rev. Neurosc. Visual input into the mushroom body Gronenberg. 2008 Myrmecol. news Olfactory input into the mushroom body oscillator Heisenberg 2003 Nature Rev. Neurosc. Visual input into the mushroom body oscillator Webb and Wystrach 2006. Cur. Opin. Ins. Sci Oscillatory model for route following Oscillator model OSCILLATOR MUSHROOM VISUAL BODIES RECEPTORS Kenyon Cells N=20,000 OSCILLATOR Projection MB Neurons N=360 Output Neuron N=1 Reinforcer Neuron N=1 LeMoël and Wystrach in prep Emergence of new behaviours Route following Taxis Oscillations Oscillations Same neural mechanisms Different behaviours! Three different angles 1. Observations of behaviours Ecological task Fine motor pattern 3. Neural implementation Neurobiology 2. Cracking the algorithm Neural models Behavioural Hypothetised algorithm experimentation Unexpected prediction Neural model of path integration Stone et al., 2007 Current biology The experimental approach is ahead… Visual sequence learning Chameron et al., 1998. PRSB Directional cue integration Wystrach et al., 2015, PRSB Visuo – motor association Beugnon et al., 2016, JCPA Route optimisation and aversive memories Wystrach et al., in prep Homing from novel locations Wystrach et al., 2012 JEB Encoding wind direction Navigation while walking backwards Wystrach et al., 2012, Cur. Biol. Schwarz and Wystrach 2017, Cur. Biol. Blowing experiment Wystrach and Schwarz 2013. Cur. biol. Wystrach and Schwarz 2013. Cur. biol. Wystrach and Schwarz 2013. Cur. biol. Wystrach and Schwarz 2013. Cur. biol. Wystrach and Schwarz 2013. Cur. biol. Wystrach and Schwarz 2013. Cur. biol. Clutching ! Wystrach and Schwarz 2013. Cur. biol. Front Back Side Wind detection (my left) WIND (East) Celestial compass (South) Wystrach and Schwarz 2013. Cur. biol. Front Back Side Wind detection (my left) WIND (East) Celestial compass (South) Wystrach and Schwarz 2013. Cur. biol. Webb, B., & Wystrach, A. (2016). Neural mechanisms of insect navigation. Current Opinion in Insect Science, 15, 27-39. How can ants follow a route backward ? Schwarz et al. 2017. Cur. biol. Schwarz et al. 2017. Cur. biol. Schwarz et al. 2017. Cur. biol. Peeking behaviour Schwarz et al. 2017. Cur. biol. Schwarz et al. 2017. Cur. biol. Schwarz et al. 2017. Cur. biol. Holonomic control Schwarz et al. 2017. Cur. biol. Not a toolkit, but a distributed system BODY / ENVIRONMENT Systematic search Scans Homing Predicting wind displacement Path integration Route following Learning walks Backward navigation from which behaviours emerge ANT TRACKBALL Pilot trials in Macquarie University, with Dr. Narendra, 2017 ANT VISUAL DISPLAY ARENA Outside view Inside view Courtesy Zoltan Kocsi VIRTUAL REALITY FOR ANTS Any possible manipulations! Sebastian Schwarz Thanks The CRCA Benjamin Risse Barbara Webb Michael Mangan Alek Khodshabashev Paul Graham The ants and larvae you Andy Philippides Konstantinos Lagogiannis now Sebastian Schwarz Mathieu Lihoreau Alix Gabrielli Audrey Dussutour Florent Lemoel Martin Giurfa Cristian Pasquaretta Guillaume Isabelle Thanks !.