Maggot learning and Synapsin function

Diegelmann, Sören; Klagges, Bert R. E.; Michels, Birgit; Schleyer, Michael; Gerber, Bertram

doi:10.1242/jeb.076208

Cited by 56 publications

(62 citation statements)

References 117 publications

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“…The current working hypothesis for associative olfactory learning in fruit flies and larvae locates the memory trace in the output synapses of the mushroom body Kenyon cells (for review, see Heisenberg 2003;Gerber et al 2009;Diegelmann et al 2013;Schleyer et al 2013). The Kenyon cells receive on the one hand odor information, on the other hand reward and punishment signals.…”

Section: Discussionmentioning

confidence: 99%

“…The larva of the fruit fly Drosophila melanogaster arguably is such a model organism. It is a well-established study case in particular for navigation tasks with respect to olfactory cues (Cobb 1999;Louis et al 2008;Gomez-Marin et al 2011;Lahiri et al 2011;Gershow et al 2012;Louis 2012, 2014;Schulze et al 2015;Wystrach et al 2016) as well as for odor-tastant learning (Scherer et al 2003;Gerber et al 2009;Diegelmann et al 2013;Schleyer et al 2013).…”

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Common microbehavioral “footprint” of two distinct classes of conditioned aversion

et al. 2017

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Avoiding unfavorable situations is a vital skill and a constant task for any animal. Situations can be unfavorable because they feature something that the animal wants to escape from, or because they do not feature something that it seeks to obtain. We investigate whether the microbehavioral mechanisms by which these two classes of aversion come about are shared or distinct. We find that larval Drosophila avoid odors either previously associated with a punishment, or previously associated with the lack of a reward. These two classes of conditioned aversion are found to be strikingly alike at the microbehavioral level. In both cases larvae show more head casts when oriented toward the odor source than when oriented away, and direct fewer of their head casts toward the odor than away when oriented obliquely to it. Thus, conditioned aversion serving two qualitatively different functions-escape from a punishment or search for a reward-is implemented by the modulation of the same microbehavioral features. These features also underlie conditioned approach, albeit with opposite sign. That is, the larvae show conditioned approach toward odors previously associated with a reward, or with the lack of a punishment. In order to accomplish both these classes of conditioned approach the larvae show fewer head casts when oriented toward an odor, and direct more of their head casts toward it when they are headed obliquely. Given that the Drosophila larva is a genetically tractable model organism that is well suited to study simple circuits at the single-cell level, these analyses can guide future research into the neuronal circuits underlying conditioned approach and aversion, and the computational principles of conditioned search and escape.

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Section: Discussionmentioning

confidence: 99%

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Common microbehavioral “footprint” of two distinct classes of conditioned aversion

et al. 2017

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“…At which stage along the olfactory pathway may such dissociation be found? We first briefly review the architecture of the olfactory pathway (for reviews, see Vosshall, 2000;Gerber and Stocker, 2007;Vosshall and Stocker, 2007;Stocker, 2008;Gerber et al, 2009;Masse et al, 2009;Touhara and Vosshall, 2009;Diegelmann et al, 2013) and then suggest two alternative scenarios for intensity learning.…”

Section: Possible Circuitry Underlying Intensity Learningmentioning

confidence: 99%

“…We tackle this issue using odour-sugar associative conditioning in larval Drosophila (Fig.1A) (Scherer et al, 2003;Michels et al, 2005;Neuser et al, 2005;Mishra et al, 2010;Chen et al, 2011;Michels et al, 2011;Saumweber et al, 2011a;Saumweber et al, 2011b) (for reviews, see Gerber and Stocker, 2007;Gerber et al, 2009;Diegelmann et al, 2013). This is a suitable system for such a study due to its simplicity in terms of cell number, its genetic tractability and the robustness of the paradigm.…”

Section: Introductionmentioning

confidence: 99%

Olfactory memories are intensity specific in larval Drosophila

Mishra

Chen

Yarali

et al. 2013

Journal of Experimental Biology

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SUMMARYLearning can rely on stimulus quality, stimulus intensity, or a combination of these. Regarding olfaction, the coding of odour quality is often proposed to be combinatorial along the olfactory pathway, and working hypotheses are available concerning short-term associative memory trace formation of odour quality. However, it is less clear how odour intensity is coded, and whether olfactory memory traces include information about the intensity of the learnt odour. Using odour-sugar associative conditioning in larval Drosophila, we first describe the dose-effect curves of learnability across odour intensities for four different odours (n-amyl acetate, 3-octanol, 1-octen-3-ol and benzaldehyde). We then chose odour intensities such that larvae were trained at an intermediate odour intensity, but were tested for retention with either that trained intermediate odour intensity, or with respectively higher or lower intensities. We observed a specificity of retention for the trained intensity for all four odours used. This adds to the appreciation of the richness in ʻcontentʼ of olfactory short-term memory traces, even in a system as simple as larval Drosophila, and to define the demands on computational models of associative olfactory memory trace formation. We suggest two kinds of circuit architecture that have the potential to accommodate intensity learning, and discuss how they may be implemented in the insect brain. Supplementary material available online at

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“…Learning and memory finetune the way an animal can act in its environment, e.g., in the search for food. Using odor-sugar reward associative learning in larval Drosophila as a study case, we investigate the role of the Synapsin protein in learning and memory (Scherer et al 2003;Neuser et al 2005;Saumweber et al 2011; for reviews, see Gerber et al 2009;Diegelmann et al 2013).…”

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Synapsin is required to “boost” memory strength for highly salient events

et al. 2015

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Synapsin is an evolutionarily conserved presynaptic phosphoprotein. It is encoded by only one gene in the Drosophila genome and is expressed throughout the nervous system. It regulates the balance between reserve and releasable vesicles, is required to maintain transmission upon heavy demand, and is essential for proper memory function at the behavioral level. Task-relevant sensorimotor functions, however, remain intact in the absence of Synapsin. Using an odor-sugar reward associative learning paradigm in larval Drosophila, we show that memory scores in mutants lacking Synapsin (syn 97 ) are lower than in wild-type animals only when more salient, higher concentrations of odor or of the sugar reward are used. Furthermore, we show that Synapsin is selectively required for larval short-term memory. Thus, without Synapsin Drosophila larvae can learn and remember, but Synapsin is required to form memories that match in strength to event salience-in particular to a high saliency of odors, of rewards, or the salient recency of an event. We further show that the residual memory scores upon a lack of Synapsin are not further decreased by an additional lack of the Sap47 protein. In combination with mass spectrometry data showing an up-regulated phosphorylation of Synapsin in the larval nervous system upon a lack of Sap47, this is suggestive of a functional interdependence of Synapsin and Sap47.

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Maggot learning and Synapsin function

Cited by 56 publications

References 117 publications

Common microbehavioral “footprint” of two distinct classes of conditioned aversion

Common microbehavioral “footprint” of two distinct classes of conditioned aversion

Olfactory memories are intensity specific in larval Drosophila

Synapsin is required to “boost” memory strength for highly salient events

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