Skip to main content
SpringerLink
Log in

Active tactile sensing for localization of objects by the cockroach antenna

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Antennal movement during tactile orientation behavior was examined three-dimensionally in American cockroaches during tethered walking. When a wooden rod was presented to the tip of one antenna in an upright orientation at one of the three different horizontal positions (30°, 60°, or 90° from the center of the head), the animal touched it repeatedly with the antenna, and tried to approach it (positive thigmotaxis). Positional shifts were also observed for the contralateral unstimulated antenna. The ipsilateral antenna tended to touch the object during inward movement (adduction) at all three test angles. The cumulative turn angle made during a continuous test period of 24 s clearly depended on the object’s position; however, the contact frequencies were almost the same regardless of the position. The relationships between contact frequency and some locomotion parameters were also investigated on a shorter time scale of 3 s. The contact frequency positively correlated with the turn angle, with the accuracy of orientation at all three test angles, and with the translation velocity at test angles of 30° and 60°. It is concluded that the performance during tactile orientation can be represented effectively by the frequency with which the antennae touch the attractive objects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Altner H, Prillinger L (1980) Ultrastructure of invertebrate chemo-, thermo, and hygroreceptors and its functional significance. Int Rev Cytol 67:69–139

    Article  Google Scholar 

  • Bell WJ (1991) Searching behaviour: the behavioural ecology of finding resources. Chapman and Hall, London

    Google Scholar 

  • Chapman RF (1982) Chemoreception: the significance of receptor numbers. Adv Insect Physiol 16:247–356

    Article  CAS  Google Scholar 

  • Comer CM, Parks L, Halvorsen MB, Breese-Terteling A (2003) The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions. J Comp Physiol A 189:97–103

    CAS  Google Scholar 

  • Dürr V, König Y, Kittmann R (2001) The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern during walking. J Comp Physiol A 187:131–144

    Article  PubMed  Google Scholar 

  • Erber J, Kierzek S, Sander E, Grandy K (1998) Tactile learning in the honeybee. J Comp Physiol A 183:737–744

    Article  Google Scholar 

  • Fanselow EE, Nicolelis MA (1999) Behavioral modulation of tactile responses in the rat somatosensory system. J Neurosci 19:7603–7616

    PubMed  CAS  Google Scholar 

  • Gentaz E, Hatwell Y (2003) Haptic processing of spatial and material object properties. In: Hatwell Y, Streri A, Gentaz E (eds) Touching for knowing: cognitive psychology of haptic manual perception. John Benjamins Publishing Company, Amsterdam, pp 123–159

    Google Scholar 

  • Gibson JJ (1962) Observations on active touch. Psychol Rev 69:477–491

    Article  PubMed  CAS  Google Scholar 

  • Hansen-Delkeskamp E (1992) Functional characterization of antennal contact chemoreceptors in the cockroach, Periplaneta americana: a electrophysiological investigation. J Insect Physiol 38:813–822

    Article  CAS  Google Scholar 

  • Hartmann MJ, Bower JM (2001) Tactile responses in the granule cell layer of cerebellar folium crus IIa of freely behaving rats. J Neurosci 21:3549–3563

    PubMed  CAS  Google Scholar 

  • Hollins M (2002) Touch and haptics. In: Yantis S (ed) Steven’s handbook of experimental psychology, vol 1. Wiley, New York, pp 585–618

  • Ikeda S, Toh Y, Okamura J, Okada J (2004) Intracellular responses of antennal chordotonal sensilla of the American cockroach. Zool Sci 21:375–383

    Article  PubMed  Google Scholar 

  • Iwamura Y, Tanaka M (1978) Postcentral neurons in hand region of area 2: their possible role in the form discrimination of tactile objects. Brain Res 150:662–666

    Article  PubMed  CAS  Google Scholar 

  • Katz D (1925) Der Aufbau der Tastwelt. Higashiyama A, Iwakiri K (trans) Shokkaku no sekai, Shinyosha, Tokyo (Japanese, 2003)

  • Keil TA, Steinbrecht RA (1984) Mechanosensitive and olfactory sensilla of insects. In: King RC, Akai H (eds) Insect ultrastructure, vol 2. Plenum Press, New York, pp 477–516

  • Kevan P, Lane MA (1985) Flower pedal microtexture is a tactile cue for bees. Proc Natl Acad Sci USA 82:4750–4752

    Article  PubMed  Google Scholar 

  • Krause AF, Dürr V (2004) Tactile efficiency of insect antennae with two hinge joints. Biol Cybern 91:168–181

    Article  PubMed  Google Scholar 

  • Lederman SJ, Klatzky RL (1987) Hand movements: a window into haptic object recognition. Cogn Psychol 19:342–368

    Article  CAS  Google Scholar 

  • Lederman SJ, Klatzky RL (1996) Action for perception: manual exploratory movements for haptically processing objects and their features. In: Wing AM, Haggard P, Flanagan JR (eds) Hand and brain: the neurophysiology and psychology of hand movements. Academic, New York, pp 431–446

    Google Scholar 

  • Lederman SJ, Klatzky RL (1998) The hand as a perceptual system. In: Connolly KJ (ed) The psychobiology of the hand. Mac Keith Press, London, pp 16–35

    Google Scholar 

  • Lee J-K, Strausfeld NJ (1990) Structure, distribution and number of surface sensilla and their receptor cells on the olfactory appendages of the male moth Manduca sexta. J Neurocytol 19:519–538

    Article  PubMed  CAS  Google Scholar 

  • Levenberg K (1944) A method for the solution of certain problems in least squares. Q Appl Math 2:164–168

    Google Scholar 

  • Marquardt D (1963) An algorithm for least-squares estimation of nonlinear parameters. SIAM J Appl Math 11:431–441

    Article  Google Scholar 

  • Martin H, Lindauer M (1966) Sinnesphysiologische Leistungen beim Wabenbau der Honigbiene. Z Vergl Physiol 53:372–404

    Article  Google Scholar 

  • Norris D, Chu H-M (1974) Morphology and ultrastructure of the antenna of male Periplaneta americana as related to chemoreception. Cell Tissue Res 150:1–9

    Article  PubMed  CAS  Google Scholar 

  • 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 186:849–857

    Article  PubMed  CAS  Google Scholar 

  • Okada J, Toh Y (2001) Peripheral representation of antennal orientation by the scapal hair plate of the cockroach Periplaneta americana. J Exp Biol 204:4301–4309

    PubMed  CAS  Google Scholar 

  • Okada J, Toh Y (2004) Spatio-temporal patterns of antennal movements in the searching cockroach. J Exp Biol 207:3693–3706

    Article  PubMed  Google Scholar 

  • Okada J, Kanamaru Y, Toh Y (2002) Mechanosensory control of antennal movement by scapal hair plates in the American cockroach. Zool Sci 19:1201–1210

    Article  PubMed  Google Scholar 

  • Pelletier Y, McLeod CD (1994) Obstacle perception by insect antennae during terrestrial locomotion. Physiol Entomol 19:360–362

    Article  Google Scholar 

  • Rüth E (1976) Elektrophysiologie der Sensilla Chaetica auf den Antennen von Periplaneta americana. J Comp Physiol A 105:55–64

    Article  Google Scholar 

  • Saager F, Gewecke M (1989) Antennal reflexes in the desert locust Schistocerca gregaria. J Exp Biol 147:519–532

    Google Scholar 

  • Schafer R, Sanchez TV (1973) Antennal sensory system of the cockroach, Periplaneta americana: postembryonic development and morphology of the sense organs. J Comp Neurol 149:335–354

    Article  PubMed  CAS  Google Scholar 

  • Schaller D (1978) Antennal sensory system of Periplaneta americana L.: distribution and frequency of morphologic types of sensilla and their sex-specific changes during postembryonic development. Cell Tissue Res 191:121–139

    Article  PubMed  CAS  Google Scholar 

  • Scheiner R, Schnitt S, Erber J (2005) The functions of antennal mechanoreceptors and antennal joints in tactile discrimination of the honeybee (Apis mellifera L.). J Comp Physiol A 191:857–864

    Article  Google Scholar 

  • Schneider D (1964) Insect antennae. Ann Rev Entomol 8:103–122

    Article  Google Scholar 

  • Seelinger G, TobinTR (1981) Sense organs. In: Bell WJ, Adiyodi KG (eds) The american cockroach. Chapman & Hall, London, pp 217–245

    Google Scholar 

  • Steinbrecht RA (1984) Chemo-, hygro-, and thermoreceptors. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument, vol 1. Springer, Berlin Heidelberg New York, pp 523–553

    Google Scholar 

  • Toh Y (1977) Fine structure of antennal sense organs of the male cockroach, Periplaneta americana. J Ultrastruct Res 60:373–394

    Article  PubMed  CAS  Google Scholar 

  • Toh Y (1981) Fine structure of sense organs on the antennal pedicel and scape of the male cockroach, Periplaneta americana. J Ultrastruct Res 77:119–132

    Article  PubMed  CAS  Google Scholar 

  • Zacharuk RY (1985) Antennae and sensilla. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 6. Pergamon Press, Oxford, pp 1–69

  • Zeil J, Sandeman R, Sandeman DC (1985) Tactile localization: the function of active antennal movements in the crayfish Cherax destructor. J Comp Physiol A 157:607–617

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Dr. S. R. Shaw (Dalhousie University, Halifax, Canada) for reading the manuscript and giving valuable comments and to Mr. J. Wakamatsu for his helpful assistance. This study was supported in part by a Grant-in-Aid for Scientific Research on Priority Areas (A) from the MEXT (12048216), a Grant-in-Aid for Young Scientists from the JSPS (14740463), and the Narishige Zoological Science Award.

Author information

Authors and Affiliations

  1. Department of Biology, Graduate School of Sciences, Kyushu University, 812-8581, Fukuoka, Japan

    Jiro Okada & Yoshihiro Toh

Authors
  1. Jiro Okada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshihiro Toh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiro Okada.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Okada, J., Toh, Y. Active tactile sensing for localization of objects by the cockroach antenna. J Comp Physiol A 192, 715–726 (2006). https://doi.org/10.1007/s00359-006-0106-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-006-0106-9

Keywords

Search

Navigation