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PreprintCited by 201Memory and Neural MechanismsNeurobiology and Insect Physiology ResearchMemory Processes and Influences

Massed and Spaced Learning in Honeybees: The Role of CS, US, the Intertrial Interval, and the Test Interval

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Menzel, Randolf, Manz, Gisela, Menzel, Rebecca, Greggers, Uwe·2001·Learning & Memory
DOI 10.1101/lm.40001PMC PMC311375
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Abstract

Conditioning the proboscis extension reflex of harnessed honeybees (Apis mellifera) is used to study the effect temporal spacing between successive conditioning trials has on memory. Retention is monitored at two long-term intervals corresponding to early (1 and 2 d after conditioning) and late long-term memory (3 and 4 d). The acquisition level is varied by using different conditioned stimuli (odors, mechanical stimulation, and temperature increase at the antenna), varying strengths of the unconditioned stimulus (sucrose), and various numbers of conditioning trials. How learning trials are spaced is the dominant factor both for acquisition and retention, and although longer intertrial intervals lead to better acquisition and higher retention, the level of acquisition per se does not determine the spacing effect on retention. Rather, spaced conditioning leads to higher memory consolidation both during acquisition and later, between the early and long-term memory phases. These consolidation processes can be selectively inhibited by blocking protein synthesis during acquisition.

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  • Spaced training leads to improved memory in invertebrates such as Aplysia californica, Drosophila melanogaster and bees, and in rodents and non-human primates.

    “Spaced training also leads to improved memory in invertebrates, such as the mollusk Aplysia californica11–14, Drosophila melanogaster15,16 and bees17, and in rodents18,19 and non-human primates20,21.”

    From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [17]

  • In honeybee olfactory learning, efficient spaced training can occur with intervals as short as 1 minute.

    “For example, in honeybee olfactory learning, efficient spaced training can occur with intervals as short as 1 minute17.”

    From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [17]

  • Even for systems such as honeybee olfactory learning that involve short, spaced intervals, effective long-term memory formation relies on activation of transcription and translation, downstream of the intracellular signalling pathways activated by these intervals.

    “However, it is evident that even for systems such as honeybee olfactory learning that involve short, spaced intervals, effective long-term memory formation relies on the activation of transcription and translation, downstream of the intracellular signalling pathways that are activated by these intervals17,70.”

    From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [17]

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Research works printed but not linked: 3

  1. Eisenhardt, D., Kreß, H., and Menzel, R. 1999. Variability of CREB transcripts in the honeybee brain. In Göttingen Neurobiology Report 1999. Proceedings of the 1st Göttingen Conference of the German Neuroscience Society 1999. Volume II, p. 549. Thieme Verlag, Stuttgart.
  2. Squire, L.R. 1987. Memory and brain. Oxford University Press, New York.
  3. Zar, J.H. 1999. The interaction of variables was tested using log linear models and then reviewed as R × C contingency tables. In Biostatistical Analysis, pg. 718. Prentice Hall, New York. Received March 9, 2001; accepted in revised form May 14, 2001.

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Authors
Menzel, R., Manz, G., Menzel, R., & Greggers, U.
Affiliations
Freie Universität Berlin (DE)
ORCID
Menzel, Randolf
Venue
Learning & Memory
Publisher
Cold Spring Harbor Laboratory
Published
2001-07-01
Volume
8
Issue
4
Pages
198-208
ISSN
  • 1072-0502 (ISSN-L)
  • 1549-5485
DOI
10.1101/lm.40001
PMC
PMC311375
OpenAlex
W2055995144
Cited by
201
References
63
Citations by year
2026: 4 · 2025: 4 · 2024: 10 · 2023: 8 · 2022: 7 · 2021: 11 · 2020: 17 · 2019: 6 · 2018: 9 · 2017: 11 · 2016: 9 · 2015: 10 · 2014: 10 · 2013: 16 · 2012: 9
Type
posted content
Language
en
Open access
Locations
  • Learning & Memory (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
Deutsche Forschungsgemeinschaft (SFB 515)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
spaced learning, massed learning, intertrial interval, test interval, long-term memory, memory consolidation, proboscis extension response, classical conditioning, conditioned stimulus, protein synthesis inhibition, olfactory conditioning, mechanical stimulation
MeSH terms
Animals, Bees, Conditioning, Classical, Dactinomycin, Memory, Odorants, Physical Stimulation, Protein Synthesis Inhibitors, Reflex, Temperature

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