Genetic dissection of consolidated memory in Drosophila

Tully, T.; Preat, T.; Boynton, S.C.; Del Vecchio, M.

doi:10.1016/0092-8674(94)90398-0

Cited by 924Neurobiology and Insect Physiology ResearchMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

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Genetic dissection of consolidated memory in Drosophila

Tully, T., Preat, T., Boynton, S.C., Del Vecchio, M.·1994·Cell

DOI 10.1016/0092-8674(94)90398-0

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Abstract

Behavioral and pharmacological experiments in many animal species have suggested that memory is consolidated from an initial, disruptable form into a long-lasting, stable form within a few hours after training. We combined these traditional approaches with genetic analyses in Drosophila to show that consolidated memory of conditioned (learned) odor avoidance 1 day after extended training consisted of two genetically distinct, functionally independent memory components: anesthesia-resistant memory (ARM) and long-term memory (LTM). ARM decayed away within 4 days, was resistant to hypothermic disruption, was insensitive to the protein synthesis inhibitor cycloheximide (CXM), and was disrupted by the radish single-gene mutation. LTM showed no appreciable decay over 7 days, was sensitive to CXM, and was not disrupted by the radish mutation.

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Spaced 15-minute intervals were more effective than massed 1-minute intervals in inducing olfactory learning in Drosophila melanogaster, even given the same total training time.
“Spaced (15-minute) intervals were more effective than massed (1-minute) intervals in inducing olfactory learning, even given the same total training time (and thus more massed presentations)63.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [63]
Memory induced by repeated training improves when presentations are spaced over time compared to equal numbers of training exposures without spacing.
“Memory that is induced by repeated training improves when presentations are spaced over time compared to equal numbers of training exposures without spacing.”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
Cold-shock treatment 2 hrs after training abolished the massed-training elicited memory enhancement in wild-type csw transgenic flies.
“Second, we exposed these flies to a cold-shock treatment (2 min in ice water), to which ARM is resistant (Tully et al., 1994; DeZazzo and Tully, 1995), 2 hrs after training and found that it abolished the massed-training elicited memory enhancement (Figure 3D).”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
4-hr memory elicited by one-trial training was normal in wild-type csw transgenic flies.
“First, we examined 4-hr memory elicited by one-trial training, which comprises only ARM (Tully et al., 1994; DeZazzo and Tully, 1995), and observed that it was normal in these transgenic flies (Figure S10).”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
Ten consecutive learning sessions without rest (massed training) produce STM, MTM and an ARM that lasts for four days.
“whereas ten consecutive learning sessions without rest in between (called massed training) produces STM, MTM and an ARM that lasts for four days.”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994

The spacing effect is a common phenomenon in the animal kingdom.
“This augmentation in memory formation is called the spacing effect and is a common phenomenon in the animal kingdom (Ebbinghaus, 1885; Carew et al., 1972; Tully et al., 1994; Gerber et al., 1998; Beck et al., 2000; Sutton et al., 2002; Cepeda et al., 2006; Philips et al., 2007).”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
LTM, a protein synthesis-dependent memory that does not decay after seven days, can be induced with ten learning sessions if rest intervals are provided between training trials (spaced training).
“Long-term memory (LTM), a protein synthesis-dependent memory that does not decay after seven days, can be induced with ten learning sessions if rest intervals are provided between the training trials. This constitutes spaced training (For a detailed description, see Tully et al., 1994; Isabel et al., 2004; reviewed in Margulies et al., 2005).”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
The massed-training-elicited memory enhancement in wild-type csw transgenic flies is protein-synthesis dependent, a major feature of LTM.
“This documented that this memory was protein-synthesis dependent, which is a major feature of LTM (Tully et al., 1994).”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
The spacing effect has been well demonstrated in Drosophila.
“The spacing effect has been well demonstrated in Drosophila (Tully et al., 1994; Beck et al., 2000; Ho et al., 2007).”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
A single learning session in the Drosophila odor and electric shock association task elicits STM, MTM, and a partial ARM that lasts less than 24 hours.
“With the extensively characterized odor and electric shock association task (Tully and Quinn, 1985; Tully et al., 1994), a single learning session elicits short-term memory (STM), mid-term memory (MTM), and a partial anesthesia-resistant memory (ARM) that lasts less than 24 hours”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994
In Drosophila, the spacing effect is well defined phenomenologically and used as a behavioral strategy to induce protein synthesis-dependent LTM.
“In Drosophila, the spacing effect is well defined phenomenologically (Tully et al., 1994; Beck et al., 2000) and it is used as a behavioral strategy to induce protein synthesis-dependent LTM.”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Tully et al., 1994

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Authors: Tully, T., Preat, T., Boynton, S. C., & Del Vecchio, M.
Affiliations: Cold Spring Harbor Laboratory (US)
Brandeis University (US)
ORCID: Tully, T.
Venue: Cell
Publisher: Elsevier BV
Published: 1994-10
Volume: 79
Issue: 1
Pages: 35-47
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/0092-8674(94)90398-0
OpenAlex: W2023796149
Cited by: 924
References: 91
Citations by year: 2026: 16 · 2025: 29 · 2024: 44 · 2023: 32 · 2022: 28 · 2021: 31 · 2020: 21 · 2019: 27 · 2018: 34 · 2017: 35 · 2016: 33 · 2015: 34 · 2014: 26 · 2013: 42 · 2012: 34
FWCI: 10.23
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
Funders: National Institutes of Health (7r29ns025621-05, 2r01hd032245-04)
National Institute of General Medical Sciences (P01GM033205, P01GM-33205)
National Institute of Neurological Disorders and Stroke (NS-25621)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-32245)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: memory consolidation, Drosophila, odor avoidance, long-term memory, memory decay, cycloheximide, protein synthesis, memory components
MeSH terms: Animals, Avoidance Learning, Brain Chemistry, Conditioning, Classical, Cycloheximide, Drosophila, Memory, Mutation, Genes, Insect

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Genetic dissection of consolidated memory in Drosophila

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