Journal of Comparative Physiology A

, Volume 193, Issue 5, pp 523–535 | Cite as

Central gustatory projections and side-specificity of operant antennal muscle conditioning in the honeybee

Original Paper


Gustatory stimuli to the antennae, especially sucrose, are important for bees and are employed in learning paradigms as unconditioned stimulus. The present study identified primary antennal gustatory projections in the bee brain and determined the impact of stimulation of the antennal tip on antennal muscle activity and its plasticity. Central projections of antennal taste hairs contained axons of two morphologies projecting into the dorsal lobe, which is also the antennal motor centre. Putative mechanosensory axons arborised in a dorso-lateral area. Putative gustatory axons projected to a ventro-medial area. Bees scan gustatory and mechanical stimuli with their antennae using variable strategies but sensory input to the motor system has not been investigated in detail. Mechanical, gustatory, and electrical stimulation of the ipsilateral antennal tip were found to evoke short-latency responses in an antennal muscle, the fast flagellum flexor. Contralateral gustatory stimulation induced smaller responses with longer latency. The activity of the fast flagellum flexor was conditioned operantly by pairing high muscle activity with ipsilateral antennal sucrose stimulation. A proboscis reward was unnecessary for learning. With contralateral antennal sucrose stimulation, conditioning was unsuccessful. Thus, muscle activity induced by gustatory stimulation was important for learning success and conditioning was side-specific.


Operant conditioning Taste hairs Antenna Unconditioned stimulus Motoneuron 



Antennal lobe


Antennal mechanosensory and motor centre


Conditioned stimulus


Dorsal lobe


Fast flagellum flexor


Proboscis extension response


Suboesophageal ganglion


Unconditioned stimulus


  1. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 92:107–119CrossRefGoogle Scholar
  2. Bornhauser BC, Meyer EP (1997) Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect. Cell Tissue Res 287:211–221PubMedCrossRefGoogle Scholar
  3. Braun G, Bicker G (1992) Habituation of an appetitive reflex in the honeybee. J Neurophysiol 67:588–598PubMedGoogle Scholar
  4. Dacher M, Lagarrigue A, Gauthier M (2005) Antennal tactile learning in the honeybee: effect of nicotinic antagonists on memory dynamics. Neuroscience 120:37–50CrossRefGoogle Scholar
  5. Edgecomb RS, Murdock LL (1992) Central projections of axons from taste hairs on the labellum and tarsi of the blowfly, Phormia regina Meigen. J Comp Neurol 315:431–444PubMedCrossRefGoogle Scholar
  6. Eisenstein EM, Cohen MJ (1965) Learning in an isolated prothoracic insect ganglion. Anim Behav 13:104–108CrossRefGoogle Scholar
  7. Erber J (1981) Neural correlates of learning in the honeybee. Trends Neurosci. 4:270–273CrossRefGoogle Scholar
  8. Erber J, Schildberger K (1980) Conditioning of an antennal reflex to visual stimuli in bees (Apis mellifera L.). J Comp Physiol 135: 217–225CrossRefGoogle 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 181:355–365CrossRefGoogle Scholar
  10. Erber J, Kierzek S, Sander E, Grandy K (1998) Tactile learning in the honeybee. J Comp Physiol A 183:737–744CrossRefGoogle Scholar
  11. 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: 557–565PubMedCrossRefGoogle Scholar
  12. Esslen J, Kaissling KE (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphologie 83:227–251CrossRefGoogle Scholar
  13. Faber T, Joerges J, Menzel R (1999) Associative learning modifies neural representations of odors in the insect brain. Nat Neurosci 2:74–78PubMedCrossRefGoogle Scholar
  14. Faensen D (1999) Das motorische System der Bienenantenne Untersuchungen zu den motorischen Mustern und zur Rolle der beteiligten Muskeln. PhD thesis, Technische Universität Berlin, BerlinGoogle Scholar
  15. Feany MB, Quinn W G (1995) A neuropeptide gene defined by memory mutant amnesiac. Science 268:869–873PubMedCrossRefGoogle Scholar
  16. Flanagan D, Mercer AR (1989) Morphology and response characteristics of neurons in the deutocerebrum of the brain in the honeybee Apis mellifera. J Comp Physiol A 164:483–494CrossRefGoogle Scholar
  17. Giurfa M, Malun D (2004) Associative mechanosensory conditioning of the proboscis extension reflex in honeybees. Learn Mem 11:294–302PubMedCrossRefGoogle Scholar
  18. Grünewald B (1999) Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera. J Comp Physiol A 185:565–576CrossRefGoogle Scholar
  19. Guez D, Suchail S, Gauthier M, Maleszka R, Belzunces LP (2001) Contrasting effects of imidacloprid on habituation in 7- and 8-day-old honeybees (Apis mellifera). Neurobiol Learn Mem 76:183 91PubMedCrossRefGoogle Scholar
  20. Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63CrossRefGoogle Scholar
  21. Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146–156PubMedGoogle Scholar
  22. Haupt SS (2004) Antennal sucrose perception in the honey bee (Apis mellifera L.): Behaviour and electrophysiology. J Comp Physiol A 190:735–745CrossRefGoogle Scholar
  23. Haupt SS, Klemt W (2005) Habituation and dishabituation of exploratory and appetitive responses in the honey bee (Apis mellifera L.). Behav Brain Res 165:12–17PubMedCrossRefGoogle Scholar
  24. Hertel H, Maronde U (1987) The physiology and morphology of centrally projecting visual interneurons in the honeybee brain. J Exp Biol 133:301–313Google Scholar
  25. Hertel H, Schäfer S, Maronde U (1987) The physiology and morphology of visual commissures in the honeybee brain. J Exp Biol 133:283–300Google Scholar
  26. Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154:826–836CrossRefGoogle Scholar
  27. Homberg U, Müller U (1999) Neuroactive substances in the antennal lobe. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 181–206Google Scholar
  28. Horridge GA (1962) Learning of leg position by the ventral nerve cord in headless insects. Proc R Soc Lond Ser B 157:33–52Google Scholar
  29. Hoyle G (1966) An isolated ganglion-nerve-muscle preparation. J Exp Biol 44:413–429PubMedGoogle Scholar
  30. Hoyle G (1980) Learning, using natural reinforcements, in insect preparations that permit cellular neuronal analysis. J Neurobiol 11:323–354PubMedCrossRefGoogle Scholar
  31. Hoyle G (1982) Pacemaker change in a learning paradigm. In: Carpenter D (ed) Cellular pacemakers, Wiley, New York, pp 3–25Google Scholar
  32. Iwama A, Shibuya T (1998) Physiology and morphology of olfactory neurons associating with the protocerebral lobe of the honeybee brain. J Insect Physiol 44:1191–1204PubMedCrossRefGoogle Scholar
  33. Jørgensen K, Kvello P, Almaas TJ, Mustaparta H (2006) Two closely located areas in the suboesophageal ganglion and the tritocerebrum receive projections of gustatory receptor neurons located on the antennae and the proboscis in the moth Heliothis virescens. J Comp Neurol 496:121–134PubMedCrossRefGoogle Scholar
  34. Kisch J, Erber J (1999) Operant conditioning of antennal movements in the honey bee. Behav Brain Res 99:93–102PubMedCrossRefGoogle Scholar
  35. Kloppenburg P (1995) Anatomy of the antennal motoneurons in the brain of the honeybee (Apis mellifera). J Comp Neurol 363:333–343PubMedCrossRefGoogle Scholar
  36. Kloppenburg P, Kirchhof BS, Mercer AR (1999) Voltage-activated currents from adult honeybee (Apis mellifera) antennal motor neurons recorded in vitro and in situ. J Neurophysiol 81:39–48PubMedGoogle Scholar
  37. Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348:583–595PubMedCrossRefGoogle Scholar
  38. Kuwabara M (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J Fac Sci Hokkaido Univ Ser VI Zool 13:458–464Google Scholar
  39. Lacher V (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxyd, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne (Apis mellifica L.). Z Vergl Phys 48:587–623CrossRefGoogle Scholar
  40. Maronde U (1991) Common projection areas of antennal and visual pathways in the honeybee brain, Apis mellifera. J Comp Neurol 309:328–340PubMedCrossRefGoogle Scholar
  41. Marshall J (1935) On the sensitivity of the chemoreceptors on the antenna and fore-tarsus of the honey-bee, Apis mellifica L. J Exp Biol 12:17–26Google Scholar
  42. Martin H, Lindauer M (1966) Sinnesphysiologische Leistungen beim Wabenbau der Honigbiene. Z Vergl Phys 53:372–404CrossRefGoogle Scholar
  43. Mauelshagen J (1993) Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J Neurophysiol 69:609–624PubMedGoogle Scholar
  44. Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62PubMedCrossRefGoogle Scholar
  45. Menzel R, Müller U (1996) Learning and memory in honeybees: from behaviour to neural substates. Annu Rev Neurosci 19:379–404PubMedCrossRefGoogle Scholar
  46. Murphey RK, Possidente D, Pollack G, Merritt D (1989) Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila. J Comp Neurol 290:185–200PubMedCrossRefGoogle Scholar
  47. Newland PL (1999) Processing of gustatory information by spiking local interneurons in the locust. J Neurophysiol 82:3149–3159PubMedGoogle Scholar
  48. Nishino H, Yamashita S, Yamazaki Y, Nishikawa M, Yokohari F, Mizunami M (2003) Projection neurons originating from thermo- and hygrosensory glomeruli in the antennal lobe of the cockroach. J Comp Neurol 455:40–55PubMedCrossRefGoogle Scholar
  49. Page RE, Erber J, Fondrk MK (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 182:489–500PubMedCrossRefGoogle Scholar
  50. Pankiw T, Page RE (1999) The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 185:207–213PubMedCrossRefGoogle Scholar
  51. Persson MG, Nässel DR (1999) Neuropeptides in insect sensory neurones: tachykinin-, FMRFamide- and allatotropin-relatd peptides in terminals of locust thoracic sensory afferents. Brain Res 816:131–141PubMedCrossRefGoogle Scholar
  52. Pribbenow B, Erber J (1996) Modulation of antennal scanning in the honeybee by sucrose stimuli, serotonin, and octopamine: behavior and electrophysiology. Neurobiol Learn Mem 66:109–120PubMedCrossRefGoogle Scholar
  53. Rehder V (1989) Sensory pathways and motoneurons of the proboscis reflex in the suboesophageal ganglion of the honey bee. J Comp Neurol 279:499–513PubMedCrossRefGoogle Scholar
  54. Rehder V, Bicker G, Hammer M (1987) Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res 247:59–66CrossRefGoogle Scholar
  55. Sandoz JC, Hammer M, Menzel R (2002) Side-specificity of olfactory learning in the honeybee: US input side. Learn Mem 9:337–348PubMedCrossRefGoogle Scholar
  56. Sandoz JC, Galizia CG, Menzel R (2003) Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honeybee antennal lobes. Neuroscience 120:1137–1148PubMedCrossRefGoogle Scholar
  57. Schäfer S, Rehder V (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43–58PubMedCrossRefGoogle Scholar
  58. Scheiner R (2001) Sucrose responsiveness and behaviour in honey bees (Apis mellifera L.). PhD thesis, Technische Universität Berlin, BerlinGoogle Scholar
  59. Scheiner R (2004) Responsiveness to sucrose and habituation of the proboscis extension response in honey bees. J Comp Physiol A 190:727–733CrossRefGoogle Scholar
  60. Scheiner R, Erber J, Page RE (1999) Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). J Comp Physiol A 185:1–10PubMedCrossRefGoogle Scholar
  61. Scheiner R, Page RE, Erber J (2001) Responsiveness to sucrose affects tactile and olfactory learning in preforaging honey bees of two genetic strains. Behav Brain Res 120:67–73PubMedCrossRefGoogle Scholar
  62. Scheiner R, Kuritz-Kaiser A, Menzel R, Erber J (2005a) Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees. Learn Mem 12: 626–635CrossRefGoogle Scholar
  63. Scheiner R, Schnitt S, Erber J (2005b) The functions of antennal mechanoreceptors and antennal joints in tactile discrimination of the honeybee (Apis mellifera L.). J Comp Physiol A 191: 857–864CrossRefGoogle Scholar
  64. Schneider D (1964) Insect antennae. Annu Rev Entomol 9:103–122CrossRefGoogle Scholar
  65. Schürmann FW, Erber J (1990) FMRFamide-like immunoreactivity in the brain of the honeybee (Apis mellifera). a light- and electron microscopical study. Neuroscience 38:797–807PubMedCrossRefGoogle Scholar
  66. Schürmann FW, Klemm N (1984) Serotonin-immunoreactive neurones in the brain of the honeybee. J Comp Neurol 225:570–580PubMedCrossRefGoogle Scholar
  67. Schürmann FW, Elekes K, Geffard M (1989) Dopamine-like immunoreactivity in the bee brain. Cell Tissue Res 256:399–410CrossRefGoogle Scholar
  68. Sinakevich I, Niwa M, Strausfeld NJ (2005) Octopamine-like immunoreactivity in the honey bee and cockroach: comparable organization in the brain and subesophageal ganglion. J Comp Neurol 488:233–254CrossRefGoogle Scholar
  69. Suzuki H (1975) Antennal movements induced by odor and central projections of the antennal neurons in the honey bee. J Insect Physiol 21:831–847CrossRefGoogle Scholar
  70. Takeda K (1961) Classically conditioned response in the honey bee. J Insect Physiol 6:168–179CrossRefGoogle Scholar
  71. Tezze A, Farina WM (1999) Trophallaxis in the honeybee, Apis mellifera: the interaction between viscosity and sucrose concentration of the transferred solution. Anim Behav 57:1319–1326PubMedCrossRefGoogle Scholar
  72. Whitehead AT, Larsen JR (1976) Ultrastructure of the contact chemoreceptors of Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 5:301–315CrossRefGoogle Scholar
  73. Woollacott M, Hoyle G (1977) Neural events underlying learning: changes in pacemaker. Proc R Soc Lond Ser B 195:395–415CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Neurobiologie, Institut für ÖkologieBerlinGermany
  2. 2.Molecular Neuroscience Unit, OIST-PC IRP, OITCOkinawaJapan

Personalised recommendations