Rapid Consolidation to a<i>radish</i>and Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning in<i>Drosophila</i>

Krashes, Michael J.; Waddell, Scott

doi:10.1523/jneurosci.5333-07.2008

Cited by 255 publications

(402 citation statements)

References 70 publications

(156 reference statements)

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“…Amnesiac is a putative neuropeptide whose release probably would be impacted by shi ts1 on a slower time scale. Indeed there is some evidence that longer-duration blocking of shi ts1 in DPM neurons can ablate performance fully (39,40), an effect that, by definition, includes both ASM and ARM.…”

Section: Resultsmentioning

confidence: 99%

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

Lee

Lin

Chang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

128

151

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Pavlovian olfactory learning in Drosophila produces two genetically distinct forms of intermediate-term memories: anesthesia-sensitive memory, which requires the amnesiac gene, and anesthesiaresistant memory (ARM), which requires the radish gene. Here, we report that ARM is specifically enhanced or inhibited in flies with elevated or reduced serotonin (5HT) levels, respectively. The requirement for 5HT was additive with the memory defect of the amnesiac mutation but was occluded by the radish mutation. This result suggests that 5HT and Radish protein act on the same pathway for ARM formation. Three supporting lines of evidence indicate that ARM formation requires 5HT released from only two dorsal paired medial (DPM) neurons onto the mushroom bodies (MBs), the olfactory learning and memory center in Drosophila: (i) DPM neurons were 5HT-antibody immunopositive; (ii) temporal inhibition of 5HT synthesis or release from DPM neurons, but not from other serotonergic neurons, impaired ARM formation; (iii) knocking down the expression of d5HT1A serotonin receptors in α/β MB neurons, which are innervated by DPM neurons, inhibited ARM formation. Thus, in addition to the Amnesiac peptide required for anesthesia-sensitive memory formation, the two DPM neurons also release 5HT acting on MB neurons for ARM formation.brain | olfaction | aversive conditioning | neurotransmitter P avlovian olfactory learning in Drosophila involves coincidence detection of a conditioned stimulus (CS), an odor, and an unconditioned stimulus (US), an electric shock (1). After one session of aversive olfactory conditioning, flies can form short-and intermediate-term memories but not long-term memory (LTM), which requires repetitive spaced training and is dependent on protein synthesis (2, 3). The intermediate-term memory has been dissected further into an anesthesia-sensitive form (ASM) that requires a gene called "amnesiac" and an anesthesia-resistant form (ARM) that requires the radish gene (4-6). Three hours after one session of training, ARM and ASM contribute equally to performance and can be distinguished by application of a short cold shock-induced anesthesia that impairs ASM but not ARM. Importantly, although ARM is consolidated, in the sense that it is resistant to cold shock, it is not thought to be a protein synthesisdependent memory because it is resistant to cycloheximide (CXM) (2). One day after repetitive spaced training, both ARM and LTM are thought to contribute to memory performance. In contrast, repetitive massed training without rest intervals induces only radish-dependent ARM without detectable cAMP response element binding protein-dependent LTM measured 1 d after training (2, 3) (but see ref.2 for an alternative model). Thus, more than one genetically distinct memory-storage system contributes to performance both at intermediate time points (e.g., 3 h after one training session) and at later time points (e.g., 24 h after repetitive training). Given the complexity of memory consolidation observed at the genetic level, much effor...

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Section: Resultsmentioning

confidence: 99%

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

Lee

Lin

Chang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

128

151

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“…For example, crammer mutant flies were reported to either show 12 or not show 13 an appetitive short term memory deficit with identical memory retention scores, because the scores of the control “CS” flies were different in the two studies. Our results further emphasize the need for a more systematic scheme addressing control populations.…”

Section: Discussionmentioning

confidence: 99%

Sub-strains of Drosophila Canton-S differ markedly in their locomotor behavior

Colomb

Brembs

2014

F1000Res

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We collected five sub-strains of the standard laboratory wild-type Drosophila melanogaster Canton Special (CS) and analyzed their walking behavior in Buridan's paradigm using the CeTrAn software. According to twelve different aspects of their behavior, the sub-strains fit into three groups. The group separation appeared not to be correlated with the origin of the stocks. We conclude that founder effects but not laboratory selection likely influenced the gene pool of the sub-strains. The flies’ stripe fixation was the parameter that varied most. Our results suggest that differences in the genome of laboratory stocks can render comparisons between nominally identical wild-type stocks meaningless. A single source for control strains may settle this problem.

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“…The water maze is a learning paradigm characterized by a motivation to escape from water, whereas the MAZE test used in the current study is a learning paradigm characterized by motivation to receive a reward. It has been reported that appetitive long-term memory (LTM) is consolidated more quickly than aversive LTM [36,37]. Moreover, Hirano et al showed that different LTM systems are utilized in the hungry state [38].…”

Section: Discussionmentioning

confidence: 99%

Perinatal exposure to genistein, a soy phytoestrogen, improves spatial learning and memory but impairs passive avoidance learning and memory in offspring

Kohara

Kuwahara

Kawaguchi

et al. 2014

Physiology & Behavior

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This study investigated the effects of perinatal genistein (GEN) exposure on the central nervous system of rat offspring. Pregnant dams orally received GEN (1 or 10 mg/kg/day) or vehicle (1 ml/kg/day) from gestation day 10 to postnatal day 14. In order to assess the effects of GEN on rat offspring, we used a battery of behavioral tests, including the open-field, elevated plus-maze, MAZE and step-through passive avoidance tests. MAZE test is an appetite-motivation test, and we used this mainly for assessing spatial learning and memory. In the MAZE test, GEN groups exhibited shorter latency from start to goal than the vehicle-treated group in both sexes. On the other hand, performances in the step-through passive avoidance test were non-monotonically inhibited by GEN in both sexes, and a significant difference was observed in low dose of the GEN-treated group compared to the vehicle-treated group in female rats. Furthermore, we found that perinatal exposure to GEN did not significantly alter locomotor activity or emotionality assessed by the open-field and elevated-plus maze tests. These results suggest that perinatal exposure to GEN improved spatial learning and memory of rat offspring, but impaired their passive avoidance learning and memory.

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Rapid Consolidation to aradishand Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning inDrosophila

Cited by 255 publications

References 70 publications

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

Serotonin–mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila

Sub-strains of Drosophila Canton-S differ markedly in their locomotor behavior

Perinatal exposure to genistein, a soy phytoestrogen, improves spatial learning and memory but impairs passive avoidance learning and memory in offspring

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