Memory through metamorphosis in normal and mutant Drosophila

Tully, Tim; Cambiazo, Verónica; Kruse, Line Riis

doi:10.1523/jneurosci.14-01-00068.1994

Cited by 166 publications

(139 citation statements)

References 57 publications

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“…Overall, our data indicate that memory enhancement begins between 1 and 3 h after single cycle training and reverts to normal within 4 days after spaced training. These results are entirely consistent with a model where memory enhancement in DC0 B3 /ϩ and DC0 H2 /ϩ flies consists of a specific increase in ARM (25).…”

Section: Dc0/؉ Mutations Do Not Affect Ltm and Enhance Arm Independentlysupporting

confidence: 90%

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Protein kinase A inhibits a consolidated form of memory in Drosophila

Horiuchi

Naganos²,

Aigaki³

et al. 2008

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

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Increasing activity of the cAMP/protein kinase A (PKA) pathway has often been proposed as an approach to improve memory in various organisms. However, here we demonstrate that singlepoint mutations, which decrease PKA activity, dramatically improve aversive olfactory memory in Drosophila. These mutations do not affect formation of early memory phases or of protein synthesis-dependent long-term memory but do cause a significant increase in a specific consolidated form of memory, anesthesiaresistant memory. Significantly, heterozygotes of null mutations in PKA are sufficient to cause this memory increase. Expressing a PKA transgene in the mushroom bodies, brain structures critical for memory formation in Drosophila, reduces memory back to wildtype levels. These results indicate that although PKA is critical for formation of several memory phases, it also functions to inhibit at least one memory phase.anesthesia-resistant memory ͉ DC0 gene ͉ learning ͉ behavior

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Section: Dc0/؉ Mutations Do Not Affect Ltm and Enhance Arm Independentlysupporting

confidence: 90%

“…Seven hours after a single cycle of training, shorter forms of memory have decayed, leaving ARM as the predominant remaining memory phase (21). The second form of consolidated memory, LTM, forms only after multiple spaced trainings for aversive associations (25).…”

Section: Identification Of Specific Point Mutations That Improve Memorymentioning

confidence: 99%

Protein kinase A inhibits a consolidated form of memory in Drosophila

Horiuchi

Naganos²,

Aigaki³

et al. 2008

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

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“…This was further confirmed with another allele, rut 2080 . Similarly, dnc 1 , defective in cAMP phosphodiesterase activity Byers et al, 1981), showed no RI stimulation, confirming the previous results that dnc larvae showed no initial learning (Aceves-Piña and Tully et al, 1994a). Thus, the requirement of both rut and dnc activities strongly argues for the importance of cAMP signaling for larval olfactory learning.…”

Section: Importance Of the Camp Signaling Pathway And Ksupporting

confidence: 84%

“…In addition, whereas the adult brain is formed through complex reorganization during metamorphosis, the larval brain is a simple extension of the embryonic axonal plan (Nassif et al, 2003). However, despite potential advantages, learning and memory studies with the Drosophila larva have been limited (Aceves-Piña and Heisenberg et al, 1985;Tully et al, 1994a;Dukas, 1998), although a series of studies was reported recently (Scherer et al, 2003;Gerber et al, 2004a;Hendel et al, 2005;Michels et al, 2005;Neuser et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Induction of cAMP Response Element-Binding Protein-Dependent Medium-Term Memory by Appetitive Gustatory Reinforcement inDrosophilaLarvae

Honjo¹,

Furukubo-Tokunaga²

2005

J. Neurosci.

118

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The fruit fly Drosophila melanogaster has been successfully used as a model animal for the study of the genetic and molecular mechanisms of learning and memory. Although most of the Drosophila learning studies have used the adult fly, the relative complexity of its neural network hinders cellular and molecular studies at high resolution. In contrast, the Drosophila larva has a simple brain with uniquely identifiable neural networks, providing an opportunity of an attractive alternative system for elucidation of underlying mechanisms involved in learning and memory. In this paper, we describe a novel paradigm of larval associative learning with a single odor and a positive gustatory reinforcer, sucrose. Mutant analyses have suggested importance of cAMP signaling and potassium channel activities in larval learning as has been demonstrated with the adult fly. Intriguingly, larval memory produced by the appetitive conditioning lasts medium term and depends on both amnesiac and cAMP response element-binding protein (CREB). A significant part of memory was disrupted at very early phase by CREB blockade without affecting immediate learning performance. Moreover, we also show that synaptic output of larval mushroom body neurons is required for retrieval but not for acquisition and retention of the larval memory, including the CREB-dependent component.

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“…Nonexclusive mechanisms by which experience with chemical deterrents have been suggested to influence herbivores are: (1) a reduction in the herbivores' chemosensory sensitivity to the deterrent with exposure (Schoonhoven, 1969;Blaney et al, 1986); (2) habituation or reduced sensitivity to the taste and odor of the deterrent chemicals (Jermy et al, 1982;Jermy, 1987;Bernays, 1995); (3) an 'induction of feeding preferences' such that the herbivores prefer host plants containing certain chemicals to the exclusion of other adequate host plants (Jermy, 1987;Szentesi & Jermy, 1989;Bernays & Chapman, 1994;Bernays, 1995;del Campo et al, 2001) or (4) conditioning experience may involve forms of associative learning in the herbivores (Papaj & Rausher, 1983;Papaj & Prokopy, 1989). Tully et al (1994) demonstrated associative learning in response to aversive stimuli in larval Drosophila that persisted into adulthood. Reduced sensitivity, habituation, and induced preferences are unlikely in the wasp predators.…”

Section: Discussionmentioning

confidence: 99%

Larval feeding experience influences adult predator acceptance of chemically defended prey

Rayor

Munson

2002

Entomologia Exp Applicata

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Generalist predatory paper wasps, Polistes dominulus, experience plant secondary defensive compounds as developing larvae through their herbivorous lepidopteran caterpillar prey and as adults through attacking caterpillars while foraging. We evaluated the role that larval and early adult experience with unpalatable prey plays in subsequent foraging choices by adult wasps. For periods of two or four weeks, caged wasps were raised exclusively on caterpillars of either unpalatable Buckeye, Junonia coenia, that sequester substantial levels of iridoid glycosides (IG) or on Painted Lady, Vanessa cardui, that contain very low levels of IG. Wasps were then allowed to forage on both caterpillar species simultaneously. Patterns of prey capture differed significantly based on previous prey experience. Regardless of previous feeding experience, adult wasps overwhelmingly preferred to take Vanessa. Yet Junonia-experienced wasps continued to attack and take back to the nest over 50% more Junonia than did Vanessa-experienced wasps. The longer the wasps' larval experience with Junonia, the more likely they were to capture Junonia caterpillars. However, the life stage at which the wasps experienced Junonia was also influential as young adult experience with the unpalatable prey was more of a deterrent than was experience strictly as larvae for Junonia-experienced wasps. The results demonstrate that, in these predators, previous experience with deterrent chemicals during their larval development alters patterns of prey acceptability to the adult insects.

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Memory through metamorphosis in normal and mutant Drosophila

Cited by 166 publications

References 57 publications

Protein kinase A inhibits a consolidated form of memory in Drosophila

Protein kinase A inhibits a consolidated form of memory in Drosophila

Induction of cAMP Response Element-Binding Protein-Dependent Medium-Term Memory by Appetitive Gustatory Reinforcement inDrosophilaLarvae

Larval feeding experience influences adult predator acceptance of chemically defended prey

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