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Journal of Comparative Physiology A

, Volume 189, Issue 2, pp 89–96 | Cite as

The antennal system and cockroach evasive behavior. I. Roles for visual and mechanosensory cues in the response

  • S. Ye
  • V. Leung
  • A. Khan
  • Y. Baba
  • C. M. ComerEmail author
Original Paper
  • 498 Downloads

Abstract

Cockroaches escape from predators by turning and then running. This behavior can be elicited when stimuli deflect one of the rostrally located and highly mobile antennae. We analyzed the behavior of cockroaches, under free-ranging conditions with videography or tethered in a motion tracking system, to determine (1) how antennal positional dynamics influence escape turning, and (2) if visual cues have any influence on antennal mediated escape. The spatial orientation of the long antennal flagellum at the time of tactile stimulation affected the direction of resultant escape turns. However, the sign of flagellar displacement caused by touch stimuli, whether it was deflected medially or laterally for example, did not affect the directionality of turns. Responsiveness to touch stimuli, and escape turn performance, were not altered by blocking vision. However, because cockroaches first orient an antenna toward stimuli entering the peripheral visual field, turn direction can be indirectly influenced by visual input. Finally, when vision was blocked, the run phase of escape responses displayed reduced average velocities and distances traveled. Our results suggest that tactile and visual influences are integrated with previously known wind-sensory mechanisms to achieve multisensory control of the full escape response.

Keywords

Antennae Escape Insects Touch Vision 

Abbreviations

DMI

descending mechanosensory interneuron

GI

giant interneuron

MTS

motion tracking system

Notes

Acknowledgements

This work was supported by NSF grant IBN-9604629. A.K. was supported by the Undergraduate Summer Research Program of the UIC Laboratory for Integrative Neuroscience. We thank Nick Mathenia for valuable assistance.

References

  1. Baba Y, Shimozawa T (1997) Diversity of motor responses initiated by a wind stimulus in the freely moving cricket, Gryllus bimaculatus. Zool Sci 14:587–594Google Scholar
  2. Burdohan JA, Comer CM (1990) An antennal-derived mechanosensory pathway in the cockroach: descending interneurons as a substrate for evasive behavior. Brain Res 535:347–353PubMedGoogle Scholar
  3. Burdohan JA, Comer CM (1996) Cellular organization of an antennal mechanosensory pathway in the cockroach Periplaneta americana. J Neurosci 16:5830–5843PubMedGoogle Scholar
  4. Camhi JM (1984) A case study in neuroethology: the escape system of the cockroach. In: Camhi JM (ed) Neuroethology. Sinauer, Sunderland, MA, chapter 4Google Scholar
  5. Camhi JM, Nolen T (1981) Properties of the escape system of the cockroach during walking. J Comp Physiol A 128:193–201Google Scholar
  6. Camhi JM, Tom W (1978) The escape behavior of the cockroach Periplaneta americana. I. Turning response to wind puffs. J Comp Physiol A 128:193–201Google Scholar
  7. Comer CM, Dowd JP (1987) Escape turning behavior of the cockroach: changes in directionality induced by unilateral lesions of the abdominal nervous system. J Comp Physiol A 160:571–583Google Scholar
  8. Comer CM, Mara E, Murphy KA, Getman M, Mungy MC (1994) Multisensory control of escape in the cockroach Periplaneta americana. II. Patterns of touch-evoked behavior. J Comp Physiol A 174:13–26Google Scholar
  9. Comer CM, Parks LY, Halvorsen MB, Terteling, AB (2003) The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions. J Comp Physiol A (in press) DOI 10.1007/s00359–002–0384–9Google Scholar
  10. Daley DL, Delcomyn F (1980) Modulation of the excitability of cockroach giant interneurons during walking. I. Simultaneous excitation and inhibition. J Comp Physiol A 138:231–239Google Scholar
  11. Drew T (1991) Visuomotor coordination in locomotion. Curr Opin Neurobiol 1:652–657PubMedGoogle Scholar
  12. Fraser PJ (1977) Cercal ablation modifies tethered flight behaviour of cockroach. Nature 268:523–524Google Scholar
  13. Ganihar D, Libersat F, Wendler G, Camhi JM (1994) Wind-evoked evasive responses in flying cockroaches. J Comp Physiol A 175:49–65PubMedGoogle Scholar
  14. Honegger H-W (1981) A preliminary note on a new optomotor response in crickets: antennal tracking of moving targets. J Comp Physiol A 142:419–421Google Scholar
  15. Ilg UJ (1997) Slow eye movements. Prog Neurobiol 53:293–329PubMedGoogle Scholar
  16. Keegan AP, Comer CM (1993) The wind-elicited escape response of cockroaches (Periplaneta americana) is influenced by lesions rostral to the escape circuit. Brain Res 620:310–316PubMedGoogle Scholar
  17. Libersat F (1992) Modulation of flight by the giant interneurons of the cockroach. J Comp Physiol A 170:379–392Google Scholar
  18. Meyer DJ, Margiotta JF, Walcott B (1981) The shadow response of the cockroach Periplaneta americana. J Neurobiol 12:93–96PubMedGoogle Scholar
  19. Okada J, Toh Y (2000) The role of antennal hair plates in object guided tactile orientation of the cockroach (Periplaneta americana). J Comp Physiol A 186:849–857CrossRefPubMedGoogle Scholar
  20. Ritzmann RE, Pollack AJ, Hudson SE, Hyvonen A (1991) Convergence of multi-modal sensory signals at thoracic interneurons of the escape system of the cockroach, Perplaneta americana. Brain Res 563:175–183PubMedGoogle Scholar
  21. Roeder KD (1959) A physiological approach to the relation between predator and prey. Smithson Misc Collect 137:287–306Google Scholar
  22. Roeder KD (1963) Nerve cells and insect behavior, 2nd edn. Harvard University Press, Cambridge, MAGoogle Scholar
  23. Schaeffer PL, Ritzmann RE (2001) Descending influences on escape behavior and motor pattern in the cockroach. J Neurobiol 49:9–28CrossRefPubMedGoogle Scholar
  24. Schaller D (1978) Antennal sensory system of Periplaneta americana. distribution and frequency of morphologic types of sensilla and their sex-specific changes during postembryonic development. Cell Tissue Res 191:121–139PubMedGoogle Scholar
  25. Schiller PH, Tehovnik EJ (2001) Look and see: how the brain moves your eyes about. Prog Brain Res 134:127–42PubMedGoogle Scholar
  26. Stein BE, Meredith MA (1993) The merging of the senses. MIT Press, Cambridge, MAGoogle Scholar
  27. Stierle IE, Getman M, Comer CM (1994) Multisensory control of escape in the cockroach Periplaneta americana. I. Initial evidence from patterns of wind-evoked behavior. J Comp Physiol A 174:1–11Google Scholar
  28. Toh Y (1981) Fine structure of sense organs on the antennal pedicel and scape of the male cockroach, Periplaneta americana. J Ultrastruct Res 77:119–132PubMedGoogle Scholar
  29. Toh Y, Yokohari F (1985) Structure of the antennal chordotonal sensilla of the American cockroach. J Ultrastruct Res 90:124–134Google Scholar
  30. Werhan C (1984) Ocellar vision and orientation in flies. Proc R Soc Lond Ser B 222:409–411Google Scholar
  31. Ye S, Comer CM (1994) Visual cues may influence the escape responses of cockroaches. Soc Neurosci Abstr 20:1025Google Scholar
  32. Ye S, Comer CM (1996) Correspondence of escape-turning behavior with activity of descending mechanosensory interneurons in the cockroach, Periplaneta americana. J Neurosci 16:5844–5853PubMedGoogle Scholar
  33. Ye S, Dowd JP, Comer CM (1995) A motion tracking system for simultaneous recording of rapid locomotion and neural activity from an insect. J Neurosci Methods 60:199–210CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • S. Ye
    • 1
  • V. Leung
    • 1
  • A. Khan
    • 1
  • Y. Baba
    • 1
  • C. M. Comer
    • 1
    Email author
  1. 1.Laboratory of Integrative Neuroscience and Neurobiology Group, Department of Biological SciencesUniversity of Illinois at ChicagoChicagoUSA

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