Coping with Space Neophobia in Drosophila melanogaster: The Asymmetric Dynamics of Crossing a Doorway to the Untrodden

We discover and examine within a wide phylogenetic perspective spatial neophobia, avoidance of untrodden terrain, in fruit flies, in an experimental setup that reduces the gap between the field and the laboratory. In our setup, fruit flies use a natal fruit as their origin, freely exploring for days their surroundings, which consists of a mixture of trodden and untrodden terrain. The interface between trodden and untrodden is, however, reduced in our setup to a wide doorway, opened within a surrounding wall. Crossing this doorway, characterized by a sharp contrast interface between trodden and untrodden, generates a behavior whose dynamics betrays the flies' space neophobia. The moment-by-moment dynamics of crossing is remarkably similar to that reported in mouse models of anxiety. This means that neophobic behavior is either homologous across arthropods and vertebrates or, not less interesting, convergent, whereby the same behavior is mediated in the two phyla by two completely different schemata.

[1]  T. Markow The secret lives of Drosophila flies , 2015, eLife.

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

[3]  Joseph W. Barter,et al.  Basal Ganglia Outputs Map Instantaneous Position Coordinates during Behavior , 2015, The Journal of Neuroscience.

[4]  Ehud Ahissar,et al.  Learning and control of exploration primitives , 2014, Journal of Computational Neuroscience.

[5]  I. Golani,et al.  Display of individuality in avoidance behavior and risk assessment of inbred mice , 2014, Front. Behav. Neurosci..

[6]  Kyle S. Smith,et al.  Investigating habits: strategies, technologies and models , 2014, Front. Behav. Neurosci..

[7]  N. Strausfeld,et al.  Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia , 2013, Science.

[8]  Ilan Golani,et al.  The developmental dynamics of behavioral growth processes in rodent egocentric and allocentric space , 2012, Behavioural Brain Research.

[9]  R. Olberg,et al.  Visual control of prey-capture flight in dragonflies , 2012, Current Opinion in Neurobiology.

[10]  Brian L. Day,et al.  Doorway‐provoked freezing of gait in Parkinson's disease , 2012, Movement disorders : official journal of the Movement Disorder Society.

[11]  W. Barrows The Reactions Of The Pomace Fly: Drosophila Ampelophila Loew, To Odorous Substances... , 2012 .

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

[13]  Gabriel A Radvansky,et al.  Walking through Doorways Causes Forgetting: Further Explorations , 2011, Quarterly journal of experimental psychology.

[14]  Michael Brecht,et al.  Intracellular Determinants of Hippocampal CA1 Place and Silent Cell Activity in a Novel Environment , 2011, Neuron.

[15]  Y. Benjamini,et al.  Quantifying the buildup in extent and complexity of free exploration in mice , 2011, Proceedings of the National Academy of Sciences.

[16]  Gabriel A Radvansky,et al.  Walking through doorways causes forgetting: Environmental integration , 2010, Psychonomic bulletin & review.

[17]  Michael B. Reiser,et al.  Drosophila fly straight by fixating objects in the face of expanding optic flow , 2010, Journal of Experimental Biology.

[18]  Yoav Benjamini,et al.  Freedom of movement and the stability of its unfolding in free exploration of mice , 2009, Proceedings of the National Academy of Sciences.

[19]  J. Thomson,et al.  Pollinator experience, neophobia and the evolution of flowering time , 2009, Proceedings of the Royal Society B: Biological Sciences.

[20]  Jan Wessnitzer,et al.  Place memory in crickets , 2008, Proceedings of the Royal Society B: Biological Sciences.

[21]  P. Mitra,et al.  Analysis of the Trajectory of Drosophila melanogaster in a Circular Open Field Arena , 2007, PloS one.

[22]  U. Homberg,et al.  Coding of Azimuthal Directions via Time-Compensated Combination of Celestial Compass Cues , 2007, Current Biology.

[23]  M. Giurfa Faculty Opinions recommendation of Maplike representation of celestial E-vector orientations in the brain of an insect. , 2007 .

[24]  Björn Brembs,et al.  Different parameters support generalization and discrimination learning in Drosophila at the flight simulator. , 2006, Learning & memory.

[25]  M. Heisenberg,et al.  Distinct memory traces for two visual features in the Drosophila brain , 2006, Nature.

[26]  A. Graybiel The basal ganglia: learning new tricks and loving it , 2005, Current Opinion in Neurobiology.

[27]  Bruce L. McNaughton,et al.  Progressive Transformation of Hippocampal Neuronal Representations in “Morphed” Environments , 2005, Neuron.

[28]  Judy Stamps,et al.  Genotypic differences in space use and movement patterns in Drosophila melanogaster , 2005, Animal Behaviour.

[29]  Uwe Homberg,et al.  Neurons of the Central Complex of the Locust Schistocerca gregaria are Sensitive to Polarized Light , 2002, The Journal of Neuroscience.

[30]  Yoav Benjamini,et al.  Statistical discrimination of natural modes of motion in rat exploratory behavior , 2000, Journal of Neuroscience Methods.

[31]  M. Heisenberg,et al.  The memory template in Drosophila pattern vision at the flight simulator , 1999, Vision Research.

[32]  N. Strausfeld,et al.  Mushroom bodies of the cockroach: Their participation in place memory , 1998, The Journal of comparative neurology.

[33]  A. Cools,et al.  Nijmegen High and Low Responders to Novelty: A New Tool in the Search After the Neurobiology of Drug Abuse Liability , 1998, Pharmacology Biochemistry and Behavior.

[34]  A. Cools,et al.  Use of high and low responders to novelty in rat studies on the role of the ventral striatum in radial maze performance: effects of intra-accumbens injections of sulpiride. , 1993, Canadian journal of physiology and pharmacology.

[35]  I. Golani A mobility gradient in the organization of vertebrate movement: The perception of movement through symbolic language , 1992, Behavioral and Brain Sciences.

[36]  R. Strauss,et al.  Coordination of legs during straight walking and turning in Drosophila melanogaster , 1990, Journal of Comparative Physiology A.

[37]  A. Hoffmann,et al.  Selection for territoriality in Drosophila melanogaster: correlated responses in mating success and other fitness components , 1989, Animal Behaviour.

[38]  P. Best,et al.  Place cells and silent cells in the hippocampus of freely-behaving rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  Ronald C. Arkin,et al.  Motor schema based navigation for a mobile robot: An approach to programming by behavior , 1987, Proceedings. 1987 IEEE International Conference on Robotics and Automation.

[41]  R. Morris Developments of a water-maze procedure for studying spatial learning in the rat , 1984, Journal of Neuroscience Methods.

[42]  B. A. Cartwright,et al.  How honey bees use landmarks to guide their return to a food source , 1982, Nature.

[43]  R. W. Siegel,et al.  Conditioned responses in courtship behavior of normal and mutant Drosophila. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. O’Keefe,et al.  Hippocampal place units in the freely moving rat: Why they fire where they fire , 1978, Experimental Brain Research.

[45]  W. Harris,et al.  Conditioned behavior in Drosophila melanogaster. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[46]  T. Dobzhansky,et al.  ON FOOD PREFERENCES OF SYMPATRIC SPECIES OF DROSOPHILA , 1951 .

[47]  R. Ritzmann,et al.  10 Insect Walking: From Reduced Preparations to Natural Terrain , 2007 .

[48]  M. Srinivasan,et al.  Searching behaviour of desert ants, genusCataglyphis (Formicidae, Hymenoptera) , 2004, Journal of comparative physiology.

[49]  Michael A. Arbib,et al.  Sensorimotor Transformations in the Worlds of Frogs and Robots , 1995, Artif. Intell..

[50]  K. Connolly Locomotor activity in Drosophila. 3. A distinction between activity and reactivity. , 1967, Animal behaviour.

[51]  R. F. Thompson,et al.  Habituation: a model phenomenon for the study of neuronal substrates of behavior. , 1966, Psychological review.

[52]  H. Mittelstaedt Prey capture in Mantids , 1957 .

[53]  G. P. Baerends Fortpflanzungsverhalten und Orientierung der Grabwespe Ammophila campestris Jur , 1941 .