Insect Behavioral Evidence of Spatial Memories During Environmental Reconfiguration

  • Diogo Santos-PataEmail author
  • Alex Escuredo
  • Zenon Mathews
  • Paul F. M. J. Verschure
Conference paper
Part of the Lecture Notes in Computer Science book series (LNCS, volume 10928)


Insects are great explorers, able to navigate through long-distance trajectories and successfully find their way back. Their navigational routes cross dynamic environments suggesting adaptation to novel configurations. Arthropods and vertebrates share neural organizational principles and it has been shown that rodents modulate their neural spatial representation accordingly with environmental changes. However, it is unclear whether insects reflexively adapt to environmental changes or retain memory traces of previously explored situations. We sought to disambiguate between insect behavior in environmental novel situations and reconfiguration conditions. An immersive mixed-reality multi-sensory setup was built to replicate multi-sensory cues. We have designed an experimental setup where female crickets Gryllus Bimaculatus were trained to move towards paired auditory and visual cues during primarily phonotactic driven behavior. We hypothesized that insects were capable of identifying sensory modifications in known environments. Our results show that, regardless of the animal’s history, novel situation conditions did not compromise the animals performance and navigational directionality towards a new target location. However, in trials where visual and auditory stimuli were spatially decoupled, the animals heading variability towards a previously known position significantly increased. Our findings showed that crickets can behaviorally manifest environmental reconfiguration, suggesting the encoding for spatial representation.


Insect Navigation Memory Spatial representation 



The research leading to these results has received funding from the European Research Council under the European Unions Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. [341196] cDAC.

Author Contributions Statement. Z.M. and P.V. conceived the experiment, D.S.P. conducted the experiment and analyzed the results. D.S.P, Z.M., and A.E developed the setup. All authors were involved in the revision of the manuscript.


  1. 1.
    Vickers, N.J.: Mechanisms of animal navigation in odor plumes. Biol. Bull. 198(2), 203–212 (2000)CrossRefGoogle Scholar
  2. 2.
    Mathews, Z., Lechón, M., Calvo, J.B., Dhir, A., Duff, A., Verschure, P.F., et al.: Insect-like mapless navigation based on head direction cells and contextual learning using chemo-visual sensors. In: IEEE/RSJ International Conference on Intelligent Robots and Systems, IROS 2009, pp. 2243–2250. IEEE (2009)Google Scholar
  3. 3.
    Thorson, J., Weber, T., Huber, F.: Auditory behavior of the cricket. J. Comp. Physiol. 146(3), 361–378 (1982)CrossRefGoogle Scholar
  4. 4.
    Mizunami, M., Weibrecht, J.M., Strausfeld, N.J.: Mushroom bodies of the cockroach: their participation in place memory. J. Comp. Neurol. 402(4), 520–537 (1998)CrossRefGoogle Scholar
  5. 5.
    Wessnitzer, J., Mangan, M., Webb, B.: Place memory in crickets. Proc. R. Soc. Lond. B Biol. Sci. 275(1637), 915–921 (2008)CrossRefGoogle Scholar
  6. 6.
    Srinivasan, M.V., Poteser, M., Kral, K.: Motion detection in insect orientation and navigation. Vis. Res. 39(16), 2749–2766 (1999)CrossRefGoogle Scholar
  7. 7.
    Zhang, S., Mizutani, A., Srinivasan, M.V.: Maze navigation by honeybees: learning path regularity. Learn. Mem. 7(6), 363–374 (2000)CrossRefGoogle Scholar
  8. 8.
    Skinner, B.F.: The Behavior of Organisms: An Experimental Analysis (1938)Google Scholar
  9. 9.
    Von Frisch, K.: The Dance Language and Orientation of Bees (1967)Google Scholar
  10. 10.
    Nieh, J.C.: A negative feedback signal that is triggered by peril curbs honey bee recruitment. Curr. Biol. 20(4), 310–315 (2010)CrossRefGoogle Scholar
  11. 11.
    Dacke, M., Srinivasan, M.V.: Evidence for counting in insects. Anim. Cogn. 11(4), 683–689 (2008)CrossRefGoogle Scholar
  12. 12.
    Dill, M., Wolf, R., Heisenberg, M.: Visual pattern recognition in drosophila involves retinotopic matching. Nature 365(6448), 751 (1993)CrossRefGoogle Scholar
  13. 13.
    Collett, T., Fauria, K., Dale, K., Baron, J.: Places and patternsa study of context learning in honeybees. J. Comp. Physiol. A 181(4), 343–353 (1997)CrossRefGoogle Scholar
  14. 14.
    Brembs, B., Wiener, J.: Context and occasion setting in drosophila visual learning. Learn. Mem. 13(5), 618–628 (2006)CrossRefGoogle Scholar
  15. 15.
    Horseman, G., Huber, F.: Sound localisation in crickets. J. Comp. Physiol. A 175(4), 399–413 (1994)CrossRefGoogle Scholar
  16. 16.
    Huber, F.: Central nervous control of sound production in crickets and some speculations on its evolution. Evolution 16, 429–442 (1962)CrossRefGoogle Scholar
  17. 17.
    Walker, T.J.: Specificity in the response of female tree crickets (orthoptera, gryllidae, oecanthinae) to calling songs of the males. Ann. Entomol. Soc. Am. 50(6), 626–636 (1957)CrossRefGoogle Scholar
  18. 18.
    Latimer, W., Lewis, D.: Song harmonic content as a parameter determining acoustic orientation behaviour in the cricketteleogryllus oceanicus (le guillou). J. Comp. Physiol. A 158(4), 583–591 (1986)CrossRefGoogle Scholar
  19. 19.
    Wendler, G., Dambach, M., Schmitz, B., Scharstein, H.: Analysis of the acoustic orientation behavior in crickets (gryllus campestris l.). Naturwissenschaften 67(2), 99–101 (1980)CrossRefGoogle Scholar
  20. 20.
    Kramer, E.: Orientation of the male silkmoth to the sex attractant bombykol. Olfaction Taste 5, 329–335 (1975)Google Scholar
  21. 21.
    Weber, T., Thorson, J., Huber, F.: Auditory behavior of the cricket. J. Comp. Physiol. 141(2), 215–232 (1981)CrossRefGoogle Scholar
  22. 22.
    Honegger, H.-W.: A preliminary note on a new optomotor response in crickets: antennal tracking of moving targets. J. Comp. Physiol. 142(3), 419–421 (1981)CrossRefGoogle Scholar
  23. 23.
    Kammerer, R., Bauer, W., Honegger, H.: On-line analysis of rapid motion with a microcomputer. J. Neurosci. Methods 19(2), 89–94 (1987)CrossRefGoogle Scholar
  24. 24.
    Domnisoru, C., Kinkhabwala, A.A., Tank, D.W.: Membrane potential dynamics of grid cells. Nature 495(7440), 199–204 (2013)CrossRefGoogle Scholar
  25. 25.
    Emoto, S., Ando, N., Takahashi, H., Kanzaki, R.: Insect-controlled robot-evaluation of adaptation ability. J. Robot. Mechatron. 19(4), 436 (2007)CrossRefGoogle Scholar
  26. 26.
    Shiramatsu, D., Ando, N., Takahashi, H., Kanzaki, R., Fujita, S., Sano, Y., Andoh, T.: Target selection mechanism for collision-free navigation of robots based on antennal tracking strategies of crickets. In: 2010 3rd IEEE RAS and EMBS International Conference on Biomedical Robotics and Biomechatronics (BioRob), pp. 259–264. IEEE (2010)Google Scholar
  27. 27.
    Kleindienst, H.-U., Wohlers, D.W., Larsen, O.N.: Tympanal membrane motion is necessary for hearing in crickets. J. Comp. Physiol. 151(4), 397–400 (1983)CrossRefGoogle Scholar
  28. 28.
    Morris, R.: Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11(1), 47–60 (1984)CrossRefGoogle Scholar
  29. 29.
    Leutgeb, J.K., Leutgeb, S., Moser, M.-B., Moser, E.I.: Pattern separation in the dentate gyrus and ca3 of the hippocampus. Science 315(5814), 961–966 (2007)CrossRefGoogle Scholar
  30. 30.
    Tolman, E.C.: Cognitive maps in rats and men. Psychol. Rev. 55(4), 189 (1948)CrossRefGoogle Scholar
  31. 31.
    O’keefe, J., Nadel, L.: The Hippocampus as a Cognitive Map, vol. 3. Clarendon Press, Oxford (1978)Google Scholar
  32. 32.
    Strausfeld, F., Nicholas, J., Hirth, F.: Deep homology of arthropod central complex and vertebrate basal ganglia. Science 340(6129), 157–161 (2013)CrossRefGoogle Scholar
  33. 33.
    Tomer, R., Denes, A.S., Tessmar-Raible, K., Arendt, D.: Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142(5), 800–809 (2010)CrossRefGoogle Scholar
  34. 34.
    Hirth, F., Reichert, H.: BioEssaysGoogle Scholar
  35. 35.
    Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., Moser, E.I.: Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052), 801–806 (2005)CrossRefGoogle Scholar
  36. 36.
    Taube, J.S.: Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15(1), 70–86 (1995)CrossRefGoogle Scholar
  37. 37.
    Homberg, U.: In search of the sky compass in the insect brain. Naturwissenschaften 91(5), 199–208 (2004)CrossRefGoogle Scholar
  38. 38.
    Mathews, Z., et al.: Generic neuromorphic principles of cognition and attention for ants, humans and real-world artefacts: a comparative computational approach (2011)Google Scholar
  39. 39.
    Rinderer, T.E., Baxter, J.R.: Honey bee hoarding behaviour: effects of previous stimulation by empty comb. Anim. Behav. 27, 426–428 (1979)CrossRefGoogle Scholar
  40. 40.
    Wang, Y., Kocher, S.D., Linksvayer, T.A., Grozinger, C.M., Page, R.E., Amdam, G.V.: Regulation of behaviorally associated gene networks in worker honey bee ovaries. J. Exp. Biol. 215(1), 124–134 (2012)CrossRefGoogle Scholar
  41. 41.
    Maffei, G., Santos-Pata, D., Marcos, E., Sánchez-Fibla, M., Verschure, P.F.: An embodied biologically constrained model of foraging: from classical and operant conditioning to adaptive real-world behavior in DAC-X. Neural Netw. 72, 88–108 (2015)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Diogo Santos-Pata
    • 1
    • 2
    Email author
  • Alex Escuredo
    • 1
    • 2
  • Zenon Mathews
    • 2
  • Paul F. M. J. Verschure
    • 1
    • 2
    • 3
  1. 1.SPECS, Institute for Bioengineering of CataloniaBarcelonaSpain
  2. 2.SPECS, Univesitat Pompeu FabraBarcelonaSpain
  3. 3.Institució Catalana de Recerca i Estudis Avanats (ICREA)BarcelonaSpain

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