JRM Vol.33 No.3 pp. 494-504
doi: 10.20965/jrm.2021.p0494


Auditory Virtual Reality for Insect Phonotaxis

Noriyasu Ando*1,*2, Hisashi Shidara*3, Naoto Hommaru*4, and Hiroto Ogawa*3

*1Department of Systems Life Engineering, Maebashi Institute of Technology
460-1 Kamisadori-cho, Maebashi, Gunma 371-0816, Japan

*2Research Center for Advanced Science and Technology, The University of Tokyo
4-6-1 Komaba, Meguro-ku, Tokyo 153-8904, Japan

*3Department of Biological Sciences, Faculty of Science, Hokkaido University
Kita 10, Nishi 8, Kita-ku, Sapporo 060-0810, Japan

*4Graduate School of Life Science, Hokkaido University
Kita 10, Nishi 8, Kita-ku, Sapporo 060-0810, Japan

January 19, 2021
April 14, 2021
June 20, 2021
insect navigation, cricket, virtual reality, phonotaxis, audition

Insects have a sophisticated ability to navigate real environments. Virtual reality (VR) is a powerful tool for analyzing animal navigation in laboratory studies and is the most successful when used in the study of visually guided behaviors. However, the use of VR with non-visual sensory information, such as sound, on which nocturnal insects rely, for analyzing animal navigation has not been fully studied. We developed an auditory VR for the study of auditory navigation in crickets, Gryllus bimaculatus. The system consisted of a spherical treadmill on which a tethered female cricket walked. Sixteen speakers were placed around the cricket for auditory stimuli. The two optical mice attached to the treadmill measured the cricket’s locomotion, and the sound pressure and direction of the auditory stimuli were controlled at 100 Hz based on the position and heading of the cricket relative to a sound source in a virtual arena. We demonstrated that tethered female crickets selectively responded to the conspecific male calling song and localized the sound source in a virtual arena, which was similar to the behavior of freely walking crickets. Further combinations of our system with neurophysiological techniques will help understand the neural mechanisms for insect auditory navigation.

A cricket in the auditory virtual reality

A cricket in the auditory virtual reality

Cite this article as:
N. Ando, H. Shidara, N. Hommaru, and H. Ogawa, “Auditory Virtual Reality for Insect Phonotaxis,” J. Robot. Mechatron., Vol.33 No.3, pp. 494-504, 2021.
Data files:
  1. [1] B. Webb, “Robots in invertebrate neuroscience,” Nature, Vol.417, No.6886, pp. 359-363, 2002.
  2. [2] B. Webb, “Robots with insect brains,” Science, Vol.368, No.6488, 244, 2020.
  3. [3] F. Huber, T. E. Moore et al., “Cricket Behavior and Neurobiology,” Cornell University Press, 1989.
  4. [4] H. H. Wilson, T. Mito et al., “The Cricket as a Model Organism,” Springer Japan, 2017.
  5. [5] B. Hedwig, “Pulses, patterns and paths: neurobiology of acoustic behaviour in crickets,” J. Comp. Physiol. A, Vol.192, No.7, pp. 677-689, 2006.
  6. [6] B. Webb, “Using robots to model animals: A cricket test,” Robot. Auton. Syst., Vol.16, Nos.2-4, pp. 117-134, 1995.
  7. [7] B. Webb, R. R. Harrison et al., “Sensorimotor control of navigation in arthropod and artificial systems,” Arthropod Struct. Dev., Vol.33, No.3, pp. 301-329, 2004.
  8. [8] B. Hedwig, “Trackball Systems for Analysing Cricket Phonotaxis,” H. H. Wilson, T. Mito et al. (Eds.), “The Cricket as a Model Organism,” Springer Japan, pp. 303-312, 2017.
  9. [9] T. Weber, J. Thorson et al., “Auditory-behavior of the cricket. 1. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill,” J. Comp. Physiol., Vol.141, No.2, pp. 215-232, 1981.
  10. [10] B. Hedwig, “A highly sensitive opto-electronic system for the measurement of movements,” J. Neurosci. Meth., Vol.100, Nos.1-2, pp. 165-171, 2000.
  11. [11] M. Oe and H. Ogawa, “Neural basis of stimulus-angle-dependent motor control of wind-elicited walking behavior in the cricket Gryllus bimaculatus,” PLOS ONE, Vol.8, No.11, e80184, 2013.
  12. [12] H. Bohm, K. Schildberger et al., “Visual and acoustic course control in the cricket Gryllus bimaculatus,” J. Exp. Biol., Vol.159, pp. 235-248, 1991.
  13. [13] H. Haberkern and B. Hedwig, “Behavioural integration of auditory and antennal stimulation during phonotaxis in the field cricket Gryllus bimaculatus,” J. Exp. Biol., Vol.219, Issue 22, pp. 3575-3586, 2016.
  14. [14] E. Staudacher and K. Schildberger, “Gating of sensory responses of descending brain neurones during walking in crickets,” J. Exp. Biol., Vol.201, No.4, pp. 559-572, 1998.
  15. [15] K. Schildberger, “Behavioral and neuronal mechanisms of cricket phonotaxis,” Experientia, Vol.44, No.5, pp. 408-415, 1988.
  16. [16] E. Roth, S. Sponberg et al., “A comparative approach to closed-loop computation,” Curr. Opin. Neurobiol., Vol.25, pp. 54-62, 2014.
  17. [17] D. A. Dombeck and M. B. Reiser, “Real neuroscience in virtual worlds,” Curr. Opin. Neurobiol., Vol.22, No.1, pp. 3-10, 2012.
  18. [18] H. Naik, R. Bastien et al., “Animals in virtual environments,” IEEE Trans. Vis. Comput. Graph., Vol.26, No.5, pp. 2073-2083, 2020.
  19. [19] B. A. Radvansky and D. A. Dombeck, “An olfactory virtual reality system for mice,” Nat. Commun., Vol.9, No.1, 839, 2018.
  20. [20] C. A. Hernandez-Reyes, S. Fukushima et al., “Identification of exploration and exploitation balance in the silkmoth olfactory search behavior by information-Theoretic modeling,” Front. Comput. Neurosci., Vol.15, 629380, 2021.
  21. [21] P. K. Kaushik, M. Renz et al., “Characterizing long-range search behavior in Diptera using complex 3D virtual environments,” Proc. Natl. Acad. Sci., Vol.117, No.22, pp. 12201-12207, 2020.
  22. [22] A. Yamashita, N. Ando et al., “Closed-loop locomotion analyzer for investigating context-dependent collision avoidance systems in insects,” J. Robot. Soc., Vol.27, No.7, pp. 704-710, 2011.
  23. [23] D. Santos-Pata, A. Escuredo et al., “Insect behavioral evidence of spatial memories during environmental reconfiguration,” V. Vouloutsi, J. Halloy et al. (Eds.), “Biomimetic and Biohybrid Systems,” Springer International Publishing, pp. 415-427, 2018.
  24. [24] A. Funamizu, B. Kuhn et al., “Neural substrate of dynamic Bayesian inference in the cerebral cortex,” Nat. Neurosci., Vol.19, 1682, 2016.
  25. [25] S. Emoto, N. Ando et al., “Insect-controlled robot – evaluation of adaptation ability,” J. Robot. Mechatron., Vol.19, No.4, pp. 436-443, 2007.
  26. [26] N. Ando, S. Emoto et al., “Insect-controlled robot: a mobile robot platform to evaluate the odor-tracking capability of an insect,” J. Vis. Exp., Vol.118, No.118, e54802, 2016.
  27. [27] A. Miyashita, H. Kizaki et al., “No effect of body size on the frequency of calling and courtship song in the two-spotted cricket, Gryllus bimaculatus,” PLOS ONE, Vol.11, No.1, e0146999, 2016.
  28. [28] L. W. Simmons, “The calling song of the field cricket, Gryllus bimaculatus (deGeer) – Constraints on transmission and its role in intermale competition and female choice,” Anim. Behav., Vol.36, pp. 380-394, 1988.
  29. [29] B. Hedwig and J. E. A. Poulet, “Mechanisms underlying phonotactic steering in the cricket Gryllus bimaculatus revealed with a fast trackball system,” J. Exp. Biol., Vol.208, No.5, pp. 915-927, 2005.
  30. [30] N. Hommaru, H. Shidara et al., “Internal state transition to switch behavioral strategies in cricket phonotaxis,” J. Exp. Biol., Vol.223, Issue 22, jeb229732, 2020.
  31. [31] J. F. Stout, C. H. Dehaan et al., “Attractiveness of the male Acheta domesticus calling song to females. 1. Dependence on each of the calling song features,” J. Comp. Physiol., Vol.153, No.4, pp. 509-521, 1983.
  32. [32] G. Horseman and F. Huber, “Sound localisation in crickets,” J. Comp. Physiol. A, Vol.175, No.4, pp. 399-413, 1994.
  33. [33] K. Kostarakos, M. Hartbauer et al., “Matched filters, mate choice and the evolution of sexually selected traits,” PLOS ONE, Vol.3, No.8, e3005, 2008.
  34. [34] S. Hirtenlehner and H. Romer, “Selective phonotaxis of female crickets under natural outdoor conditions,” J. Comp. Physiol. A, Vol.200, No.3, pp. 239-250, 2014.
  35. [35] F. Steinbeck, A. Adden et al., “Connecting brain to behaviour: a role for general purpose steering circuits in insect orientation?,” J. Exp. Biol., Vol.223, Issue 5, jeb212332, 2020.
  36. [36] S. Schoneich and B. Hedwig, “Hyperacute directional hearing and phonotactic steering in the cricket (Gryllus bimaculatus deGeer),” PLOS ONE, Vol.5, No.12, e15141, 2010.
  37. [37] K. M. Seagraves and B. Hedwig, “Phase shifts in binaural stimuli provide directional cues for sound localisation in the field cricket Gryllus bimaculatus,” J. Exp. Biol., Vol.217, Issue 13, pp. 2390-2398, 2014.
  38. [38] B. Hedwig and J. F. A. Poulet, “Complex auditory behaviour emerges from simple reactive steering,” Nature, Vol.430, No.7001, pp. 781-785, 2004.
  39. [39] K. Kai, H. Shidara et al., “Neural activity in the central complex of the crickets during phonotaxis,” Abstr. Soc. Neurosci., 694.604, 2019.
  40. [40] M. Minderer, C. D. Harvey et al., “Neuroscience: Virtual reality explored,” Nature, Vol.533, No.7603, pp. 324-325, 2016.
  41. [41] K. Makino, N. Ando et al., “Auditory-visual virtual reality for the study of multisensory integration in insect navigation,” U. Martinez-Hernandez, V. Vouloutsi et al. (Eds.), “Biomimetic and Biohybrid Systems,” Springer, pp. 325-328, 2019.

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