A Cost of Long-Term Memory in
            <i>Drosophila</i>

Mery, Frédéric; Kawecki, Tadeusz J.

doi:10.1126/science.1111331

Cited by 264 publications

(257 citation statements)

References 4 publications

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“…Thus, it may be advantageous for for R larvae to quickly form an association between a new food source and odor and then use this new information to assess the quality of future food sources. Decreased memory retention may be advantageous for rovers, as previous studies suggest that formation and retention of formed associations can be energetically costly (Dukas 1999;Mery and Kawecki 2005;Barnard et al 2006). Conversely, staying longer in a single food patch may result in a delay in the ability to form an association between a food source and odor in for s larvae.…”

Section: Discussionmentioning

confidence: 88%

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Kaun

Hendel²,

Gerber³

et al. 2007

Learn. Mem.

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Animals must be able to find and evaluate food to ensure survival. The ability to associate a cue with the presence of food is advantageous because it allows an animal to quickly identify a situation associated with a good, bad, or even harmful food. Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we investigate whether natural variation in the foraging (for) gene in Drosophila melanogaster larvae is important in mediating associations between either an odor or a light stimulus and food reward. We found that for influences olfactory conditioning and that the mushroom bodies play a role in this for-mediated olfactory learning. Genotypes associated with high activity of the product of for, cGMP-dependent protein kinase (PKG), showed greater memory acquisition and retention compared with genotypes associated with low activity of PKG when trained with three conditioning trials. Interestingly, increasing the number of training trials resulted in decreased memory retention only in genotypes associated with high PKG activity. The difference in the dynamics of memory acquisition and retention between variants of for suggests that the ability to learn and retain an association may be linked to the foraging strategies of the two variants.Learned associations such as identifying odors as indicators of food, or showing preferences for food-related odors, are conserved across diverse taxa from humans and mice to slugs, honeybees, and fruit flies (Ache and Young 2005). The fruit fly Drosophila melanogaster can use odors as cues for the presence of both a food reward and an aversive stimulus (Tempel et al. 1983;Scherer et al. 2003;Schwaerzel et al. 2003;Margulies et al. 2005;McGuire et al. 2005;Kim et al. 2007). Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we use classical reward conditioning to investigate how natural variation in the foraging (for) gene affects acquisition and decay of memory in D. melanogaster larvae.for encodes a cGMP-dependent protein kinase (PKG) (Osborne et al. 1997). In mammals, PKG is important for proper induction of long-term potentiation (LTP) and long-term depression (LTD) (Hartell 1994;Zhuo et al. 1994;Lev-Ram et al. 1997;Arancio et al. 2001;Fiel et al. 2003Fiel et al. , 2005Kleppisch et al. 2003;Hofmann et al. 2006). Although LTP and LTD are thought to be important mechanisms underlying learning and memory (Whitlock et al. 2006), few studies have shown a direct role for PKG in learning and memory. This study aims to do this by investigating how learning differs between allelic variants of for in Drosophila larvae.for is an ideal candidate to study how natural genetic variation can affect learning and memory, since natural for variants exist that have subtle but significant variations in PKG activity (Osborne et al. 1997). The rover variants of for (for R ) have higher for transcript levels and higher PKG activities compared with the sitter variants of for (for s ) (Osb...

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Section: Discussionmentioning

confidence: 88%

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Kaun

Hendel²,

Gerber³

et al. 2007

Learn. Mem.

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show abstract

“…For example, learning a new association of color with food caused bumblebees to perform errors in a previously learned task (interference) (Worden et al, 2005). Similarly, flies that had been selected for learning ability showed a trade-off between short-and long-term memory (Mery et al, 2007), a cost of long-term memory in terms of stress resistance (Mery and Kawecki, 2005), productivity (egg laying rate) when subjected to nutritional stress (Mery and Kawecki, 2004), and larval competitive ability (Mery and Kawecki, 2003).…”

Section: B Learningmentioning

confidence: 99%

Chapter 5 Insights for Behavioral Ecology from Behavioral Syndromes

Sih

Bell

2008

Advances in the Study of Behavior

535

466

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“…The classic method to assess a role for new protein synthesis in memory is to feed animals the protein synthesis inhibitor CXM before or after training. A CXM feeding regimen was established in Drosophila that results in an ϳ50% decrease in overall protein synthesis , and this protocol has subsequently been used by several groups (Ge et al, 2004;Mery and Kawecki, 2005;Yu et al, 2006). However, our appetitive conditioning protocol requires that the flies are food deprived before training, and therefore we could not administer CXM in a glucose solution without compromising acquisition (data not shown).…”

Section: A Single Appetitive Training Session Forms Memory That Requimentioning

confidence: 99%

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

Krashes¹,

Waddell²

2008

J. Neurosci.

254

362

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In Drosophila, formation of aversive olfactory long-term memory (LTM) requires multiple training sessions pairing odor and electric shock punishment with rest intervals. In contrast, here we show that a single 2 min training session pairing odor with a more ethologically relevant sugar reinforcement forms long-term appetitive memory that lasts for days. Appetitive LTM has some mechanistic similarity to aversive LTM in that it can be disrupted by cycloheximide, the dCreb2-b transcriptional repressor, and the crammer and tequila LTMspecific mutations. However, appetitive LTM is completely disrupted by the radish mutation that apparently represents a distinct mechanistic phase of consolidated aversive memory. Furthermore, appetitive LTM requires activity in the dorsal paired medial neuron and mushroom body ␣Ј␤Ј neuron circuit during the first hour after training and mushroom body ␣␤ neuron output during retrieval, suggesting that appetitive middle-term memory and LTM are mechanistically linked. Last, experiments feeding and/or starving flies after training reveals a critical motivational drive that enables appetitive LTM retrieval.

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A Cost of Long-Term Memory in Drosophila

Cited by 264 publications

References 4 publications

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Chapter 5 Insights for Behavioral Ecology from Behavioral Syndromes

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

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