The Central Complex as a Potential Substrate for Vector Based Navigation

Insects use path integration (PI) to maintain a home vector, but can also store and recall vector-memories that take them from home to a food location, and even allow them to take novel shortcuts between food locations. The neural circuit of the Central Complex (a brain area that receives compass and optic flow information) forms a plausible substrate for these behaviors. A recent model, grounded in neurophysiological and neuroanatomical data, can account for PI during outbound exploratory routes and the control of steering to return home. Here, we show that minor, hypothetical but neurally plausible, extensions of this model can additionally explain how insects could store and recall PI vectors to follow food-ward paths, take shortcuts, search at the feeder and re-calibrate their vector-memories with experience. In addition, a simple assumption about how one of multiple vector-memories might be chosen at any point in time can produce the development and maintenance of efficient routes between multiple locations, as observed in bees. The central complex circuitry is therefore well-suited to allow for a rich vector-based navigational repertoire.

[1]  R. Wehner,et al.  The ant’s estimation of distance travelled: experiments with desert ants, Cataglyphis fortis , 2003, Journal of Comparative Physiology A.

[2]  Matthias Wittlinger,et al.  How to find home backwards? Navigation during rearward homing of Cataglyphis fortis desert ants , 2016, Journal of Experimental Biology.

[3]  Michael H. Dickinson,et al.  Idiothetic Path Integration in the Fruit Fly Drosophila melanogaster , 2017, Current Biology.

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

[5]  A. Cheung,et al.  Which coordinate system for modelling path integration? , 2010, Journal of theoretical biology.

[6]  R. Wehner,et al.  The Visual Orientation of Desert Ants, Cataglyphis bicolor, by Means of Terrestrial Cues , 1972 .

[7]  R. Vickerstaff,et al.  Published by The Company of Biologists 2005 doi:10.1242/jeb.01772 Evolving neural models of path integration , 2022 .

[8]  G. Pyke,et al.  THE FLIGHT DIRECTIONALITY OF BUMBLEBEES - DO THEY REMEMBER WHERE THEY CAME FROM , 1992 .

[9]  Allen Cheung,et al.  Animal path integration: a model of positional uncertainty along tortuous paths. , 2014, Journal of theoretical biology.

[10]  Allen Cheung,et al.  Finding the Way with a Noisy Brain , 2010, PLoS Comput. Biol..

[11]  P. Schmid-Hempel,et al.  Life duration and turnover of foragers in the antCataglyphis Bicolor (Hymenoptera, Formicidae) , 1984, Insectes Sociaux.

[12]  Harald Wolf,et al.  Establishing food site vectors in desert ants , 2012, Journal of Experimental Biology.

[13]  J. Zeil,et al.  Mapping the navigational knowledge of individually foraging ants, Myrmecia croslandi , 2013, Proceedings of the Royal Society B: Biological Sciences.

[14]  Matthew D. M. Pawley,et al.  Way-finding in displaced clock-shifted bees proves bees use a cognitive map , 2014, Proceedings of the National Academy of Sciences.

[15]  Antoine Wystrach,et al.  Views, landmarks, and routes: how do desert ants negotiate an obstacle course? , 2011, Journal of Comparative Physiology A.

[16]  A. Chiang,et al.  Visualizing Long-Term Memory Formation in Two Neurons of the Drosophila Brain , 2012, Science.

[17]  M. Lihoreau,et al.  Evidence of trapline foraging in honeybees , 2016, Journal of Experimental Biology.

[18]  R. Wehner,et al.  Pinpointing food sources: olfactory and anemotactic orientation in desert ants, Cataglyphis fortis. , 2000, The Journal of experimental biology.

[19]  B. Webb,et al.  How Ants Use Vision When Homing Backward , 2017, Current Biology.

[20]  R. Wehner,et al.  Calibration processes in desert ant navigation: vector courses and systematic search , 2002, Journal of Comparative Physiology A.

[21]  R. Wehner,et al.  How flexible is the systematic search behaviour of desert ants? , 2009, Animal Behaviour.

[22]  Thomas S. Collett,et al.  How do insects use path integration for their navigation? , 2000, Biological Cybernetics.

[23]  T S Collett,et al.  Novel landmark-guided routes in ants , 2007, Journal of Experimental Biology.

[24]  Antoine Wystrach,et al.  Ants might use different view-matching strategies on and off the route , 2012, Journal of Experimental Biology.

[25]  T. Labhart,et al.  Neural mechanisms in insect navigation: polarization compass and odometer , 2002, Current Opinion in Neurobiology.

[26]  H. A. McCartney,et al.  Compensation for wind drift by bumble-bees , 1999, Nature.

[27]  Jay Hirsh,et al.  A Pair of Dopamine Neurons Target the D1-Like Dopamine Receptor DopR in the Central Complex to Promote Ethanol-Stimulated Locomotion in Drosophila , 2010, PloS one.

[28]  T. Collett,et al.  Insect Navigation: What Backward Walking Reveals about the Control of Movement , 2017, Current Biology.

[29]  B. Webb,et al.  Neural mechanisms of insect navigation. , 2016, Current opinion in insect science.

[30]  B. Webb,et al.  Spontaneous formation of multiple routes in individual desert ants (Cataglyphis velox) , 2012 .

[31]  Lars Chittka,et al.  A Simple Iterative Model Accurately Captures Complex Trapline Formation by Bumblebees Across Spatial Scales and Flower Arrangements , 2013, PLoS Comput. Biol..

[32]  Holk Cruse,et al.  No Need for a Cognitive Map: Decentralized Memory for Insect Navigation , 2011, PLoS Comput. Biol..

[33]  Lars Chittka,et al.  Continuous Radar Tracking Illustrates the Development of Multi-destination Routes of Bumblebees , 2017, Scientific Reports.

[34]  Mandyam V. Srinivasan,et al.  Path integration in insects , 2003 .

[35]  R. Wehner,et al.  Foraging strategies in individually searching ants, Cataglyphis bicolor (Hymenoptera: Formicidae) , 1983 .

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

[37]  S. W. Zhang,et al.  Error is proportional to distance measured by honeybees: Weber’s law in the odometer , 1999, Animal Cognition.

[38]  Antoine Wystrach,et al.  Backtracking behaviour in lost ants: an additional strategy in their navigational toolkit , 2013, Proceedings of the Royal Society B: Biological Sciences.

[39]  James D. Thomson,et al.  Trapline foraging by bumble bees: IV. Optimization of route geometry in the absence of competition , 2007 .

[40]  R Wehner,et al.  Path integration in desert ants, Cataglyphis fortis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Yoshinori Aso,et al.  Dopaminergic neurons write and update memories with cell-type-specific rules , 2016, eLife.

[42]  Thierry Hoinville,et al.  Optimal multiguidance integration in insect navigation , 2018, Proceedings of the National Academy of Sciences.

[43]  Thomas S. Collett,et al.  How does the insect central complex use mushroom body output for steering? , 2018, Current Biology.

[44]  Lars Chittka,et al.  Bees do not use nearest-neighbour rules for optimization of multi-location routes , 2011, Biology Letters.

[45]  V. Fourcassié,et al.  Food searching behaviour in the ant Formica schaufussi (Hymenoptera, Formicidae): response of naive foragers to protein and carbohydrate food , 1994, Animal Behaviour.

[46]  A. Reynolds,et al.  Radar Tracking and Motion-Sensitive Cameras on Flowers Reveal the Development of Pollinator Multi-Destination Routes over Large Spatial Scales , 2012, PLoS biology.

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

[48]  T. Collett,et al.  Spatial Memory in Insect Navigation , 2013, Current Biology.

[49]  Gerald M. Rubin,et al.  Neuroarchitecture of the Drosophila central complex: A catalog of nodulus and asymmetrical body neurons and a revision of the protocerebral bridge catalog , 2018, The Journal of comparative neurology.

[50]  Ken Cheng,et al.  Finding food: outbound searching behavior in the Australian desert ant Melophorus bagoti , 2013 .

[51]  R. Wehner The architecture of the desert ant's navigational toolkit (Hymenoptera: Formicidae) , 2009 .

[52]  Randolf Menzel,et al.  The memory structure of navigation in honeybees , 2015, Journal of Comparative Physiology A.

[53]  T. Collett,et al.  Calibration of vector navigation in desert ants , 1999, Current Biology.

[54]  Rüdiger Wehner,et al.  Idiosyncratic route-based memories in desert ants, Melophorus bagoti: How do they interact with path-integration vectors? , 2005, Neurobiology of Learning and Memory.

[55]  Friedrich Otto,et al.  Die Bedeutung des Rückfluges für die Richtungs- und Entfernungsangabe der Bienen , 1959, Zeitschrift für vergleichende Physiologie.

[56]  Thierry Hoinville,et al.  Learning and Retrieval of Memory Elements in a Navigation Task , 2012, Living Machines.

[57]  Alex D. M. Dewar,et al.  Still no convincing evidence for cognitive map use by honeybees , 2014, Proceedings of the National Academy of Sciences.

[58]  R. Menzel,et al.  Honey bees navigate according to a map-like spatial memory. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Zeil,et al.  How Wasps Acquire and Use Views for Homing , 2016, Current Biology.

[60]  B. Webb,et al.  An Anatomically Constrained Model for Path Integration in the Bee Brain , 2017, Current Biology.

[61]  B. Webb,et al.  Optimal cue integration in ants , 2015, Proceedings of the Royal Society B: Biological Sciences.

[62]  Antoine Wystrach,et al.  Information content of visual scenes influences systematic search of desert ants , 2013, Journal of Experimental Biology.