Skip to main content
SpringerLink
Log in

The Auditory System of the Honey Bee

  • Chapter
  • First Online:
Honeybee Neurobiology and Behavior

Abstract

The auditory organ of honey bee is the “Johnston’s organ (JO)” on the antennae which detects airborne vibration during waggle dance communication and also detects air current during flight. The sensory afferents of the JO send their axons to two distinct areas of the bee brain, the Antennal mechanosensory centers (AMMC) and the Superior posterior slope (SPS). Within these termination fields sensory axons in the ventro-medial SPS are characterized by both thick processes with large varicosities and somatotopy, while those in the AMMC by both thin processes with small varicosities and no somatotopy, suggesting that vibratory signals detected by the JO are processed in dual parallel pathways in these primary sensory centers. In order to clarify the characteristics of auditory processing, the response properties of the interneurons to the vibration stimuli, arborizing in these primary sensory centers have been investigated. AMMC-Int-1 and AMMC-Int-2 densely arborize in AMMC and respond stimulus-phase-dependently to the vibratory stimulation on the ipsilateral antenna with high sensitivity in the range of 250–300 Hz, which is the main airborne vibration frequencies generated by the waggle dance. While SPS-D-1 has dense arborizations in the SPS and sends axons into the ventral nerve cord, with blebby terminals in the contralateral dSEG and SPS, and respond to the vibratory stimulation on the ipsilateral antenna with long-lasting excitation during olfactory stimulation on the contralateral antenna. The possible roles of the parallel systems in the primary auditory centers are discussed.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AMMC:

Antennal mechanosensory and motor center

dSEG:

dorsal region of subesophageal ganglion

GABA:

Gamma amino butyric acid

HBS:

Honey bee standard brain

JO:

Johnston’s organ

SPS:

Superior posterior slope

References

  1. Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437(3):363–383

    Article  PubMed  CAS  Google Scholar 

  2. Ai H (2010) Vibration-processing interneurons in the honeybee brain. Front Syst Neurosci 3:19

    PubMed  Google Scholar 

  3. Ai H, Nishino H, Itoh T (2007) Topographic organization of sensory afferents of Johnston’s organ in the honeybee brain. J Comp Neurol 502(6):1030–1046

    Article  PubMed  Google Scholar 

  4. Ai H, Rybak J, Menzel R, Itoh T (2009) Response characteristics of vibration-sensitive interneurons related to Johnston’s organ in the honeybee, Apis mellifera. J Comp Neurol 515(2):145–160

    Article  PubMed  Google Scholar 

  5. Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege HC, Menzel R (2005) Three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492(1):1–19

    Article  PubMed  Google Scholar 

  6. Brockmann A, Robinson GE (2007) Central projections of sensory systems involved in honey bee dance language communication. Brain Behav Evol 70(2):125–136

    Article  PubMed  Google Scholar 

  7. Dreller C, Kirchner WH (1993) How honeybees perceive the information of the dance language. Naturwissenschaften 80:319–321

    Article  Google Scholar 

  8. Erber J, Schildberger K (1980) Conditioning of an antennal reflex to visual stimuli in bees (Apis mellifera L.). J Comp Physiol 135:217–225

    Article  Google Scholar 

  9. Erber J, Pribbenow B, Grandy K, Kierzek S (1997) Tactile motor learning in the antennal system of the honeybee (Apis mellifera L.). J Comp Physiol A 181:355–365

    Article  Google Scholar 

  10. Erber J, Pribbenow B, Kisch J, Faensen D (2000) Operant conditioning of antennal muscle activity in the honey bee (Apis mellifera L.). J Comp Physiol A 186(6):557–565

    Article  PubMed  CAS  Google Scholar 

  11. Farina WM, Grüter C, Diaz PC (2005) Social learning of floral odours inside the honeybee hive. Proc R Soc B 272(1575):1923–1928

    Article  PubMed  Google Scholar 

  12. Frisch Kv (ed) (1967) The tail-wagging dance as a means of communication when food sources are distant. The Dance Language and Orientation of Bees, vol 1, 1st edn. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  13. Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420

    Article  PubMed  CAS  Google Scholar 

  14. Goodman LJ, Fletcher WA, Guy RG, Mobbs PG, Pomfrett CDJ (eds) (1987) Motion sensitive descending interneurons, ocellar LD neurons and neck motoneurons in the bee: a neural substrate for visual course control in Apis mellifera., Neurobiology and behavior of honeybees, vol 1. Springer-Verlag, Berlin

    Google Scholar 

  15. Gopfert MC, Briegel H, Robert D (1999) Mosquito hearing: sound-induced antennal vibrations in male and female Aedes aegypti. J Exp Biol 202:2727–2738

    PubMed  CAS  Google Scholar 

  16. Ignell R, Dekker T, Ghaninia M, Hansson BS (2005) Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493(2):207–240

    Article  PubMed  Google Scholar 

  17. Imaizumi K, Pollack GS (2005) Central projections of auditory receptor neurons of crickets. J Comp Neurol 493(3):439–447

    Article  PubMed  Google Scholar 

  18. Kamikouchi A, Shimada T, Ito K (2006) Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J Comp Neurol 499(3):317–356

    Article  PubMed  Google Scholar 

  19. Kirchner WH, Lindauer M, Michelsen A (1988) Honeybee dance communication: Acoustical indication of direction in round dances. Naturwissenschaften 75:629–630

    Article  Google Scholar 

  20. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, Rössler W (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499(6):933–952

    Article  PubMed  Google Scholar 

  21. Maronde U (1991) Common projection areas of antennal and visual pathways in the honeybee brain, Apis mellifera. J Comp Neurol 309(3):328–340

    Article  PubMed  CAS  Google Scholar 

  22. McIver SB (ed) (1985) Mechanoreception. Comprehensive insect physiology, biochemistry and pharmacology, vol 6. Pergamon Press, Oxford

    Google Scholar 

  23. Menzel R, De Marco RJ, Greggers U (2006) Spatial memory, navigation and dance behaviour in Apis mellifera. J Comp Physiol A 192(9):889–903

    Article  PubMed  Google Scholar 

  24. Michelsen A (2003) Karl von Frisch lecture. Signals and flexibility in the dance communication of honeybees. J Comp Physiol A 189(3):165–174

    PubMed  Google Scholar 

  25. Mobbs PG (1982) The brain of the honeybee Apis mellifera. I, The connections and spatial organization of the mushroom bodies. Philos Trans E Soc Lond B 298:309–354

    Article  Google Scholar 

  26. Müller D, Abel R, Brandt R, Zöckler M, Menzel R (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188(5):359–370

    Article  PubMed  CAS  Google Scholar 

  27. Pareto A (1972) Spatial distribution of sensory antennal fibres in the central nervous system of worker bees. Z Zellforsch Mikrosk Anat 131(1):109–140

    Article  PubMed  CAS  Google Scholar 

  28. Pribbenow B, Erber J (1996) Modulation of antennal scanning in the honeybee by sucrose stimuli, serotonin, and octopamine: behavior and electrophysiology. Neurobiol Learn Mem 66(2):109–120

    Article  PubMed  CAS  Google Scholar 

  29. Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel R (2005) The flight paths of honeybees recruited by the waggle dance. Nature 435(7039):205–207

    Article  PubMed  CAS  Google Scholar 

  30. Rohrseitz K, Tautz J (1999) Honey bee dance communication: waggle run direction coded in antennal contacts? J Comp Physiol A 184:463–470

    Article  Google Scholar 

  31. Rybak J, Kuss A, Lamecker H, Zachow S, Hege HC, Lienhard M, Singer J, Neubert K, Menzel R (2010) The digital bee brain: integrating and managing neurons in a common 3D reference system. Front Syst Neurosci 4:30

    Google Scholar 

  32. Schäfer S, Bicker G (1986) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246(3):287–300

    Article  PubMed  CAS  Google Scholar 

  33. Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185

    Article  Google Scholar 

  34. Srinivasan MV, Zhang S (2004) Visual motor computations in insects. Annu Rev Neurosci 27:679–696

    Article  PubMed  CAS  Google Scholar 

  35. Suzuki H (1975) Antennal movements induced by odour and central projection of the antennal neurones in the honey-bee. J Insect Physiol 21:831–847

    Article  Google Scholar 

  36. Thom C, Gilley DC, Hooper J, Esch HE (2007) The scent of the waggle dance. PLoS Biol 5(9):e228

    Article  PubMed  Google Scholar 

  37. Tsujiuchi S, Sivan-Loukianova E, Eberl DF, Kitagawa Y, Kadowaki T (2007) Dynamic range compression in the honey bee auditory system toward waggle dance sounds. PLoS One 2(2):e234

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Biology, Department of Earth System Science, Fukuoka University, 8-19-1 Nanakuma, Jonan-ku, Fukuoka, 814-0180, Japan

    Hiroyuki Ai & Tsunao Itoh

Authors
  1. Hiroyuki Ai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tsunao Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroyuki Ai .

Editor information

Editors and Affiliations

  1. , Department of Neurobiology, Universität Konstanz, Universitätsstrasse 10, Konstanz, 78457, Germany

    C. Giovanni Galizia

  2. , Department of Neurobiology, Freie Universität Berlin, Königin-Luise-Str. 28-30, Berlin, 14195, Germany

    Dorothea Eisenhardt

  3. , Centre de Recherches sur la Cognition An, CNRS - Université Paul Sabatier, Route de Narbonne 118, Toulouse Cedex 9, 31062, France

    Martin Giurfa

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Ai, H., Itoh, T. (2012). The Auditory System of the Honey Bee. In: Galizia, C., Eisenhardt, D., Giurfa, M. (eds) Honeybee Neurobiology and Behavior. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2099-2_21

Download citation

Publish with us

Policies and ethics

Search

Navigation