Skip to main content
Log in

Effects of morphine on associative memory and locomotor activity in the honeybee (Apis mellifera)

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

Morphine can modulate the processes underlying memory in vertebrates. However, studies have shown various modulations by morphine: positive, negative and even neutral. The honeybee is a potential platform for evaluating the effects of drugs, especially addictive drugs, on the nervous system. However, the involvement of morphine in learning and memory in insects or other invertebrates is poorly understood. The current work evaluated whether morphine affects memory acquisition, consolidation and retrieval in honeybees, using the proboscis extension response (PER) paradigm. We demonstrated that morphine treatment (5 μg/bee) before training decreased the percentage of correct PERs and the response latency related to aversive rather than rewarding odors when tested after 1 or 24 h. Morphine treatment after training also caused a decrease in this latency when tested after 24 h. Meanwhile, morphine treatment reduced the ambulation distance when tested after 30 min. Our findings suggest that morphine impairs the acquisition of short- and long-term associative memory and slightly disrupts the consolidation of long-term memory in honeybees. These negative effects cannot be explained by reduced locomotion but by impaired memory associated with aversion.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Lu W, Dong HJ, Gong ZH, Su RB, Li J. Agmatine inhibits morphine-induced memory impairment in the mouse step-down inhibitory avoidance task. Pharmacol Biochem Behav 2010, 97: 256–261.

    Article  PubMed  CAS  Google Scholar 

  2. Aguilar MA, Minarro J, Simon VM. Dose-dependent impairing effects of morphine on avoidance acquisition and performance in male mice. Neurobiol Learn Mem 1998, 69: 92–105.

    Article  PubMed  CAS  Google Scholar 

  3. Tayebi Meybodi K, Vakili Zarch A, Zarrindast MR, Djahanguiri B. Effects of ultra-low doses of morphine, naloxone and ethanol on morphine state-dependent memory of passive avoidance in mice. Behav Pharmacol 2005, 16: 139–145.

    Article  PubMed  CAS  Google Scholar 

  4. Ma MX, Chen YM, He J, Zeng T, Wang JH. Effects of morphine and its withdrawal on Y-maze spatial recognition memory in mice. Neuroscience 2007, 147: 1059–1065.

    Article  PubMed  CAS  Google Scholar 

  5. Zhu F, Yan CX, Zhao Y, Li PP, Li SB. Effects of pre-training morphine on spatial memory acquisition and retrieval in mice. Physiol Behav 2011, 104: 754–760.

    Article  PubMed  CAS  Google Scholar 

  6. Farahmandfar M, Karimian SM, Naghdi N, Zarrindast MR, Kadivar M. Morphine-induced impairment of spatial memory acquisition reversed by morphine sensitization in rats. Behav Brain Res 2010, 211: 156–163.

    Article  PubMed  CAS  Google Scholar 

  7. Mariani RK, Mello CF, Rosa MM, Ceretta AP, Camera K, Rubin MA. Effect of naloxone and morphine on arcaine-induced state-dependent memory in rats. Psychopharmacology (Berl) 2011, 215: 483–491.

    Article  CAS  Google Scholar 

  8. Zarrindast MR, Piri M, Nasehi M, Ebrahimi-Ghiri M. Nitric oxide in the nucleus accumbens is involved in retrieval of inhibitory avoidance memory by nicotine. Pharmacol Biochem Behav 2012, 101: 166–173.

    Article  PubMed  CAS  Google Scholar 

  9. Rassouli Y, Rezayof A, Zarrindast MR. Role of the central amygdala GABA-A receptors in morphine state-dependent memory. Life Sci 2010, 86: 887–893.

    Article  PubMed  CAS  Google Scholar 

  10. Shiigi Y, Takahashi M, Kaneto H. Facilitation of memory retrieval by pretest morphine mediated by mu but not delta and kappa opioid receptors. Psychopharmacology (Berl) 1990, 102: 329–332.

    Article  CAS  Google Scholar 

  11. Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443: 931–949.

    Article  Google Scholar 

  12. Bitterman ME, Menzel R, Fietz A, Schafer S. Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 1983, 97: 107–119.

    Article  PubMed  CAS  Google Scholar 

  13. Menzel R, Giurfa M. Dimensions of cognition in an insect, the honeybee. Behav Cogn Neurosci Rev 2006, 5: 24–40.

    Article  PubMed  Google Scholar 

  14. Szyszka P, Galkin A, Menzel R. Associative and nonassociative plasticity in kenyon cells of the honeybee mushroom body. Front Syst Neurosci 2008, 2: 3.

    Article  PubMed  Google Scholar 

  15. Menzel R, Muller U. Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 1996, 19: 379–404.

    Article  PubMed  CAS  Google Scholar 

  16. Okada R, Rybak J, Manz G, Menzel R. Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J Neurosci 2007, 27: 11736–11747.

    Article  PubMed  CAS  Google Scholar 

  17. Hourcade B, Muenz TS, Sandoz JC, Rossler W, Devaud JM. Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain? J Neurosci 2010, 30: 6461–6465.

    Article  PubMed  CAS  Google Scholar 

  18. Denker M, Finke R, Schaupp F, Grun S, Menzel R. Neural correlates of odor learning in the honeybee antennal lobe. Eur J Neurosci 2010, 31: 119–133.

    Article  PubMed  Google Scholar 

  19. Menzel R. Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 2001, 8: 53–62.

    Article  PubMed  CAS  Google Scholar 

  20. Si A, Zhang SW, Maleszka R. Effects of caffeine on olfactory and visual learning in the honey bee (Apis mellifera). Pharmacol Biochem Behav 2005, 82: 664–672.

    Article  PubMed  CAS  Google Scholar 

  21. Barron AB, Maleszka R, Helliwell PG, Robinson GE. Effects of cocaine on honey bee dance behaviour. J Exp Biol 2009, 212: 163–168.

    Article  PubMed  Google Scholar 

  22. Hammer M, Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 1998, 5: 146–156.

    PubMed  CAS  Google Scholar 

  23. Maleszka R, Helliwell P. Effect of juvenile hormone on shortterm olfactory memory in young honeybees (Apis mellifera). Horm Behav 2001, 40: 403–408.

    Article  PubMed  CAS  Google Scholar 

  24. Si A, Helliwell P, Maleszka R. Effects of NMDA receptor antagonists on olfactory learning and memory in the honeybee (Apis mellifera). Pharmacol Biochem Behav 2004, 77: 191–197.

    Article  PubMed  CAS  Google Scholar 

  25. Maleszka R, Helliwell P, Kucharski R. Pharmacological interference with glutamate re-uptake impairs long-term memory in the honeybee, apis mellifera. Behav Brain Res 2000, 115: 49–53.

    Article  PubMed  CAS  Google Scholar 

  26. Nunez J, Almeida L, Balderrama N, Giurfa M. Alarm pheromone induces stress analgesia via an opioid system in the honeybee. Physiol Behav 1997, 63: 75–80.

    Article  PubMed  CAS  Google Scholar 

  27. Dacher M, Gauthier M. Involvement of NO-synthase and nicotinic receptors in learning in the honey bee. Physiol Behav 2008, 95: 200–207.

    Article  PubMed  CAS  Google Scholar 

  28. Nunez J, Maldonado H, Miralto A, Balderrama N. The stinging response of the honeybee: effects of morphine, naloxone and some opioid peptides. Pharmacol Biochem Behav 1983, 19: 921–924.

    Article  PubMed  CAS  Google Scholar 

  29. Bouw MR, Gardmark M, Hammarlund-Udenaes M. Pharmacokinetic-pharmacodynamic modelling of morphine transport across the blood-brain barrier as a cause of the antinociceptive effect delay in rats—a microdialysis study. Pharm Res 2000, 17: 1220–1227.

    Article  PubMed  CAS  Google Scholar 

  30. Ngai SH, Berkowitz BA, Yang JC, Hempstead J, Spector S. Pharmacokinetics of naloxone in rats and in man: basis for its potency and short duration of action. Anesthesiology 1976, 44: 398–401.

    Article  PubMed  CAS  Google Scholar 

  31. Smith BH. The olfactory memory of the honeybee Apis Mellifera: I. odorant modulation of short- and intermediate-term memory after single-trial conditioning. J Exp Biol 1991, 161: 367–382.

    Google Scholar 

  32. Riemensperger T, Voller T, Stock P, Buchner E, Fiala A. Punishment prediction by dopaminergic neurons in Drosophila. Curr Biol 2005, 15: 1953–1960.

    Article  PubMed  CAS  Google Scholar 

  33. Schroll C, Riemensperger T, Bucher D, Ehmer J, Voller T, Erbguth K, et al. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 2006, 16: 1741–1747.

    Article  PubMed  CAS  Google Scholar 

  34. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 2003, 23: 10495–10502.

    PubMed  CAS  Google Scholar 

  35. Unoki S, Matsumoto Y, Mizunami M. Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 2005, 22: 1409–1416.

    Article  PubMed  Google Scholar 

  36. Unoki S, Matsumoto Y, Mizunami M. Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning. Eur J Neurosci 2006, 24: 2031–2038.

    Article  PubMed  Google Scholar 

  37. Vergoz V, Roussel E, Sandoz JC, Giurfa M. Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS One 2007, 2: e288.

    Article  PubMed  Google Scholar 

  38. Porras G, De Deurwaerdere P, Moison D, Spampinato U. Conditional involvement of striatal serotonin3 receptors in the control of in vivo dopamine outflow in the rat striatum. Eur J Neurosci 2003, 17: 771–781.

    Article  PubMed  Google Scholar 

  39. Murphy NP, Lam HA, Maidment NT. A comparison of morphine-induced locomotor activity and mesolimbic dopamine release in C57BL6, 129Sv and DBA2 mice. J Neurochem 2001, 79: 626–635.

    Article  PubMed  CAS  Google Scholar 

  40. Roeder T, Seifert M, Kahler C, Gewecke M. Tyramine and octopamine: antagonistic modulators of behavior and metabolism. Arch Insect Biochem Physiol 2003, 54: 1–13.

    Article  PubMed  CAS  Google Scholar 

  41. Hardie SL, Zhang JX, Hirsh J. Trace amines differentially regulate adult locomotor activity, cocaine sensitivity, and female fertility in Drosophila melanogaster. Dev Neurobiol 2007, 67: 1396–1405.

    Article  PubMed  CAS  Google Scholar 

  42. Fussnecker BL, Smith BH, Mustard JA. Octopamine and tyramine influence the behavioral profile of locomotor activity in the honey bee (Apis mellifera). J Insect Physiol 2006, 52: 1083–1092.

    Article  PubMed  CAS  Google Scholar 

  43. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 1998, 80: 1–27.

    PubMed  CAS  Google Scholar 

  44. Kalivas PW, Nakamura M. Neural systems for behavioral activation and reward. Curr Opin Neurobiol 1999, 9: 223–227.

    Article  PubMed  CAS  Google Scholar 

  45. Wolf FW, Heberlein U. Invertebrate models of drug abuse. J Neurobiol 2003, 54: 161–178.

    Article  PubMed  CAS  Google Scholar 

  46. Nathanson JA, Hunnicutt EJ, Kantham L, Scavone C. Cocaine as a naturally occurring insecticide. Proc Natl Acad Sci U S A 1993, 90: 9645–9648.

    Article  PubMed  CAS  Google Scholar 

  47. McClung C, Hirsh J. Stereotypic behavioral responses to free-base cocaine and the development of behavioral sensitization in Drosophila. Curr Biol 1998, 8: 109–112.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jianhong Wang.

Additional information

These authors contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fu, Y., Chen, Y., Yao, T. et al. Effects of morphine on associative memory and locomotor activity in the honeybee (Apis mellifera). Neurosci. Bull. 29, 270–278 (2013). https://doi.org/10.1007/s12264-013-1308-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-013-1308-0

Keywords

Navigation