Rapid learning dynamics in individual honeybees during classical conditioning.

Evren Pamir, Paul Szyszka, Ricarda Scheiner, Martin P Nawrot
Author Information
  1. Evren Pamir: Bernstein Center for Computational Neuroscience Berlin, Germany ; Neuroinformatics and Theoretical Neuroscience, Institute of Biology, Freie Universität Berlin Germany ; Department Genetics of Learning and Memory, Leibniz Institute for Neurobiology Magdeburg, Germany.
  2. Paul Szyszka: Department of Biology, University of Konstanz Konstanz, Germany.
  3. Ricarda Scheiner: Department of Behavioral Physiology and Sociobiology (Zoology II), University of Würzburg Würzburg, Germany.
  4. Martin P Nawrot: Bernstein Center for Computational Neuroscience Berlin, Germany ; Neuroinformatics and Theoretical Neuroscience, Institute of Biology, Freie Universität Berlin Germany.

Abstract

Associative learning in insects has been studied extensively by a multitude of classical conditioning protocols. However, so far little emphasis has been put on the dynamics of learning in individuals. The honeybee is a well-established animal model for learning and memory. We here studied associative learning as expressed in individual behavior based on a large collection of data on olfactory classical conditioning (25 datasets, 3298 animals). We show that the group-averaged learning curve and memory retention score confound three attributes of individual learning: the ability or inability to learn a given task, the generally fast acquisition of a conditioned response (CR) in learners, and the high stability of the CR during consecutive training and memory retention trials. We reassessed the prevailing view that more training results in better memory performance and found that 24 h memory retention can be indistinguishable after single-trial and multiple-trial conditioning in individuals. We explain how inter-individual differences in learning can be accommodated within the Rescorla-Wagner theory of associative learning. In both data-analysis and modeling we demonstrate how the conflict between population-level and single-animal perspectives on learning and memory can be disentangled.

Keywords

References

  1. J Comp Physiol A. 1999 Jul;185(1):1-10 [PMID: 10450609]
  2. Neurobiol Learn Mem. 1998 Jan;69(1):71-8 [PMID: 9521816]
  3. J Comp Physiol A. 1998 Apr;182(4):489-500 [PMID: 9565478]
  4. Learn Mem. 2005 Nov-Dec;12(6):626-35 [PMID: 16322365]
  5. J Exp Biol. 2012 Apr 1;215(Pt 7):1076-83 [PMID: 22399652]
  6. Exp Gerontol. 2007 Dec;42(12):1146-53 [PMID: 17976939]
  7. Annu Rev Psychol. 2004;55:51-86 [PMID: 14744210]
  8. PLoS One. 2010 Oct 19;5(10):e13504 [PMID: 20976061]
  9. Eur J Neurosci. 2011 Jul;34(2):352-60 [PMID: 21692886]
  10. J Neurosci. 1993 Apr;13(4):1379-86 [PMID: 8463826]
  11. Front Behav Neurosci. 2010 Sep 01;4: [PMID: 20877430]
  12. Proc Natl Acad Sci U S A. 2004 Sep 7;101(36):13124-31 [PMID: 15331782]
  13. Eur J Neurosci. 1998 Aug;10(8):2742-5 [PMID: 9767405]
  14. Naturwissenschaften. 2012 Sep;99(9):677-86 [PMID: 22869163]
  15. Neuroreport. 2010 Aug 23;21(12):812-6 [PMID: 20571459]
  16. J Neurosci. 1998 Jun 1;18(11):4384-92 [PMID: 9592115]
  17. Learn Mem. 2001 Mar-Apr;8(2):53-62 [PMID: 11274250]
  18. Zoology (Jena). 2002;105(4):313-20 [PMID: 16351880]
  19. Learn Mem. 2012 Jan 17;19(2):54-66 [PMID: 22251890]
  20. J Neurosci. 2004 May 5;24(18):4460-8 [PMID: 15128860]
  21. Learn Mem. 2011 Oct 31;18(11):733-41 [PMID: 22042602]
  22. Annu Rev Entomol. 2008;53:145-60 [PMID: 17803459]
  23. J Neurosci Methods. 2012 Oct 15;211(1):159-67 [PMID: 22960052]
  24. J Neurobiol. 2003 Jan;54(1):238-53 [PMID: 12486707]
  25. C R Acad Sci III. 1995 Jul;318(7):749-55 [PMID: 7583763]
  26. J Exp Biol. 2009 Apr;212(Pt 7):994-1002 [PMID: 19282496]
  27. Learn Mem. 2012 Dec 17;20(1):29-33 [PMID: 23247252]
  28. Anim Cogn. 2010 Nov;13(6):805-15 [PMID: 20521073]
  29. PLoS One. 2012;7(6):e39349 [PMID: 22724000]
  30. J Comp Psychol. 1983 Jun;97(2):107-19 [PMID: 6872507]
  31. Behav Brain Res. 2001 Apr 8;120(1):67-73 [PMID: 11173086]
  32. Nat Rev Neurosci. 2012 Nov;13(11):758-68 [PMID: 23080415]
  33. Insects. 2014 Jun 10;5(2):377-98 [PMID: 26462690]
  34. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2003 Jun;189(6):427-34 [PMID: 12715200]
  35. Cell Mol Life Sci. 2006 May;63(9):989-98 [PMID: 16596333]
  36. Learn Mem. 2001 Jul-Aug;8(4):198-208 [PMID: 11533223]
  37. PLoS One. 2012;7(9):e45131 [PMID: 23028801]
  38. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2001 Dec;187(11):891-9 [PMID: 11866187]
  39. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2007 Aug;193(8):801-24 [PMID: 17639413]
  40. J Comput Neurosci. 2012 Apr;32(2):197-212 [PMID: 21698405]
  41. Neurobiol Learn Mem. 2011 Sep;96(2):339-52 [PMID: 21742045]
  42. Neurobiol Learn Mem. 2001 Sep;76(2):138-50 [PMID: 11502146]
  43. J Vis Exp. 2011 Jan 24;(47): [PMID: 21304470]
  44. Behav Genet. 1984 Sep;14(5):527-57 [PMID: 6395853]
  45. J Neurosci. 2011 May 18;31(20):7229-39 [PMID: 21593307]
  46. Front Behav Neurosci. 2010 Dec 31;4:192 [PMID: 21258642]
  47. J Neurosci. 2005 May 4;25(18):4485-92 [PMID: 15872095]
  48. Proc Natl Acad Sci U S A. 1974 Mar;71(3):708-12 [PMID: 4207071]
  49. Learn Mem. 2014 Apr 16;21(5):272-86 [PMID: 24741108]

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