Differences in long-term memory stability and amCREB level between forward and backward conditioned honeybees (Apis mellifera)

Johannes Felsenberg, Yan Dyck, Janina Feige, Jenny Ludwig, Jenny Aino Plath, Anja Froese, Melanie Karrenbrock, Anna Nolle, Karin Heufelder, Dorothea Eisenhardt*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)
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In classical conditioning a predictive relationship between a neutral stimulus (conditioned stimulus; CS) and a meaningful stimulus (unconditioned stimulus; US) is learned when the CS precedes the US. In backward conditioning the sequence of the stimuli is reversed. In this situation animals might learn that the CS signals the end or the absence of the US. In honeybees 30 min and 24 h following backward conditioning a memory for the excitatory and inhibitory properties of the CS could be retrieved, but it remains unclear whether a late long-term memory is formed that can be retrieved 72 h following backward conditioning. Here we examine this question by studying late long-term memory formation in forward and backward conditioning of the proboscis extension response (PER). We report a difference in the stability of memory formed upon forward and backward conditioning with the same number of conditioning trials. We demonstrate a transcription-dependent memory 72 h after forward conditioning but do not observe a 72 h memory after backward conditioning. Moreover we find that protein degradation is differentially involved in memory formation following these two conditioning protocols. We report differences in the level of a transcription factor, the cAMP response element binding protein (CREB) known to induce transcription underlying long-term memory formation, following forward and backward conditioning. Our results suggest that these alterations in CREB levels might be regulated by the proteasome. We propose that the differences observed are due to the sequence of stimulus presentation between forward and backward conditioning and not to differences in the strength of the association of both stimuli.

Original languageEnglish
Article number91
Pages (from-to)91-1-91-13
Number of pages13
JournalFrontiers in Behavioral Neuroscience
Issue numberAPR
Publication statusPublished - 27 Apr 2015
Externally publishedYes

Bibliographical note

Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.


  • Backward conditioning
  • Classical conditioning
  • CREB
  • Long-term memory
  • Proteasome
  • Transcription
  • Ubiquitin


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