A clock gene,
            <i>period</i>
            , plays a key role in long-term memory formation in
            <i>Drosophila</i>

Sakai, Tomoaki; Tamura, Tomohide; Kitamoto, Toshihiro; Kidokoro, Yoshiaki

doi:10.1073/pnas.0401472101

Cited by 143 publications

(188 citation statements)

References 41 publications

(67 reference statements)

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“…The strong expression of dNR2 in ellipsoid body interested us, as another closely-related substructure of the central complex, the fanshaped body, appears to subserve a short-term memory trace for visual learning 25 and may be involved with LTM formation after courtship conditioning 26 . We identified several GAL4 drivers with preferential expression in these dNR2-positive ellipsoid body neurons ( Fig.…”

Section: Resultsmentioning

confidence: 96%

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

et al. 2007

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In humans and many other animals, memory consolidation occurs through multiple temporal phases and usually involves more than one neuroanatomical brain system. Genetic dissection of Pavlovian olfactory learning in Drosophila melanogaster has revealed multiple memory phases, but the predominant view holds that all memory phases occur in mushroom body neurons. Here, we demonstrate an acute requirement for NMDA receptors (NMDARs) outside of the mushroom body during long-term memory (LTM) consolidation. Targeted dsRNA-mediated silencing of Nmdar1 and Nmdar2 (also known as dNR1 or dNR2, respectively) in cholinergic R4m-subtype large-field neurons of the ellipsoid body specifically disrupted LTM consolidation, but not retrieval. Similar silencing of functional NMDARs in the mushroom body disrupted an earlier memory phase, leaving LTM intact. Our results clearly establish an anatomical site outside of the mushroom body involved with LTM consolidation, thus revealing both a distributed brain system subserving olfactory memory formation and the existence of a system-level memory consolidation in Drosophila.Pavlovian olfactory learning in Drosophila creates an elemental associative memory in a simple, accessible insect brain. This form of behavioral plasticity requires the normal function of NMDARs 1 , as is the case in other invertebrate and vertebrate species 2,3 . Memory formation in flies thereafter proceeds through several temporal phases and involves multiple biochemical cascades, which is again similar to findings from other animal models 4-6 . In particular, spaced training produces stronger, longer-lasting memory than massed training, which is a common property of memory formation 7,8 . Contrary to the fact that memory storage involves multiple anatomical regions in other animal models 9 , olfactory memory has been proposed to be stored predominantly in the mushroom body neurons 5,10 .The mushroom body is a prominent neuropillar structure in the insect central brain. Intrinsic mushroom body cells send neurites ventrally into the calyx, a region of dendritic arborization that is innervated by efferents from several different regions, including projection neurons from the antennal lobes 11 . Mushroom body axons project rostrally as a densely packed and stalk-like structure called the pedunculus to the anterior face of the brain, where they split and give rise to the dorsally projecting a and a¢ lobes and the medially projecting b, b¢ and g lobes 12 . Output neurons from the mushroom body project to many parts of the central brain. Another prominent neuropil is the central complex, which consists of four substructures, the ellipsoid body, the fan-shaped body, the nodulii and the protocerebral bridge. The central complex lies in the central brain between the pedunculi of the mushroom body and is bounded laterally by the two antennoglomerular tracts, dorsally by the pars intercerebralis, ventrally by the esophagus and the great commissure and frontally by the median bundle and the b-lobes of the mushroom bodies fronta...

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Section: Resultsmentioning

confidence: 96%

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

et al. 2007

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“…One gene involved in the circadian clock system in flies and mice is Period1 (Per1) [10 -12]. Notably, the insect version of Per1, Per, is involved in circadian, learning and courtship behaviour [10,13,14].…”

Section: Introductionmentioning

confidence: 99%

The clock genePeriod1regulates innate routine behaviour in mice

et al. 2014

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Laboratory mice are well capable of performing innate routine behaviour programmes necessary for courtship, nest-building and exploratory activities although housed for decades in animal facilities. We found that in mice inactivation of the clock gene Period1 profoundly changes innate routine behaviour programmes like those necessary for courtship, nest building, exploration and learning. These results in wild-type and Period1 mutant mice, together with earlier findings on courtship behaviour in wild-type and period-mutant Drosophila melanogaster, suggest a conserved role of Period-genes on innate routine behaviour. Additionally, both per-mutant flies and Period1-mutant mice display spatial learning and memory deficits. The profound influence of Period1 on routine behaviour programmes in mice, including female partner choice, may be independent of its function as a circadian clock gene, since Period1-deficient mice display normal circadian behaviour.

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“…In this paradigm, male flies that have courted unreceptive, nonvirgin females subsequently suppress their courtship behavior, even toward receptive virgin females (17,18). The period of courtship memory retention (as evidenced by a reduction in courtship activities in males that have been aversively ''trained'' with nonvirgin females) varies in length depending on the training conditions (17,19,20). One-hour training creates memories that are detectable for a few hours (17), whereas 7-h training results in long-term memory (LTM), lasting at least 5 days (20).…”

mentioning

confidence: 99%

“…The period of courtship memory retention (as evidenced by a reduction in courtship activities in males that have been aversively ''trained'' with nonvirgin females) varies in length depending on the training conditions (17,19,20). One-hour training creates memories that are detectable for a few hours (17), whereas 7-h training results in long-term memory (LTM), lasting at least 5 days (20). Here, we show that ecdysone is induced in male flies after an experience with unreceptive, nonvirgin females, and that ecdysone signaling has a critical role in the formation of LTM.…”

mentioning

confidence: 99%

Ecdysone signaling regulates the formation of long-term courtship memory in adult Drosophila melanogaster

Ishimoto¹,

Sakai²,

Kitamoto

2009

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

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Improved survival is likely linked to the ability to generate stable memories of significant experiences. Considerable evidence in humans and mammalian model animals shows that steroid hormones, which are released in response to emotionally arousing experiences, have an important role in the consolidation of memories of such events. In insects, ecdysone is the major steroid hormone, and it is well characterized with respect to its essential role in coordinating developmental transitions such as larval molting and metamorphosis. However, the functions of ecdysone in adult physiology remain largely elusive. Here, we show that 20-hydroxyecdysone (20E), the active metabolite of ecdysone that is induced by environmental stimuli in adult Drosophila, has an important role in the formation of long-term memory (LTM). In male flies, the levels of 20E were found to be significantly increased after courtship conditioning, and exogenous administration of 20E either enhanced or suppressed courtship LTM, depending on the timing of its administration. We also found that mutants in which ecdysone signaling is reduced were defective in LTM, and that an elevation of 20E levels was associated with activation of the cAMP response element binding protein (CREB), an essential regulator of LTM formation. Our results demonstrate that the molting steroid hormone ecdysone in adult Drosophila is critical to the evolutionarily conserved strategy that is used for the formation of stable memories. We propose that ecdysone is able to consolidate memories possibly by recapturing molecular and cellular processes that are used for normal neural development.courtship conditioning ͉ CREB ͉ ecdysone receptor ͉ steroid hormone ͉ 20-hydroxyecdysone

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A clock gene, period , plays a key role in long-term memory formation in Drosophila

Cited by 143 publications

References 41 publications

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body

The clock genePeriod1regulates innate routine behaviour in mice

Ecdysone signaling regulates the formation of long-term courtship memory in adult Drosophila melanogaster

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