Cellular site and molecular mode of synapsin action in associative learning

Michels, Birgit; Chen, Yi Chun; Saumweber, Timo; Mishra, Dushyant; Tanimoto, Hiromu; Schmid, Benjamin; Engmann, Olivia; Gerber, Bertram

doi:10.1101/lm.2101411

Cited by 49 publications

(58 citation statements)

References 81 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…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

Self Cite

View full text Add to dashboard Cite

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

show abstract

Section: Introductionmentioning

confidence: 99%

Olfactory memories are intensity specific in larval Drosophila

Mishra

Chen

Yarali

et al. 2013

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

show abstract

“…S1A,B). Comparing our procedures to the published ones, however, revealed that we had used a substantially lower concentration of n-amylacetate (AM) (a 1:1600 dilution rather than the 1:50 dilution of AM used in both Michels et al 2005Michels et al , 2011. Subsequently using the higher concentration of AM (1:50), the published defect of the syn 97 mutant was reproduced (Supplemental Fig.…”

mentioning

confidence: 92%

“…In Drosophila, Synapsin is encoded by only one gene and is expressed in most if not all neurons of both the larval and adult nervous system (coding gene: syn, CG 3985: Klagges et al 1996;Michels et al 2005). Both adult and larval Drosophila lacking Synapsin show associative memory scores that are reduced by about half as compared with wild-type animals, as do animals upon an RNAi-mediated knockdown of Synapsin (adult odor-punishment memory: Godenschwege et al 2004;Knapek et al 2010;Niewalda et al 2015;Walkinshaw et al 2015; larval odor-reward memory: Michels et al 2005Michels et al , 2011. Corresponding phenotypes in learning and memory tasks have been reported throughout the animal kingdom, including man (Silva et al 1996;Garcia et al 2004;Südhof, 2004;Gitler et al 2008;Greco et al 2013).…”

mentioning

confidence: 99%

“…Notably, phosphorylation seems to be important in the mode of operation of Synapsin (Angers et al 2002;Fiumara et al 2004;Giachello et al 2010;Michels et al 2011;Sadanandappa et al 2013). The working hypothesis for Synapsin function is that the type I adenylate cyclase (coding gene: rut, CG9533) detects a coincidence of odor-induced activity in mushroom body neurons on the one hand, and of an internal aminergic reinforcement signal on the other hand, such that the cAMP-PKA cascade is activated in an odor-specific subset of mushroom body neurons (Tomchik and Davis 2009;Gervasi et al 2010).…”

mentioning

confidence: 99%

“…The working hypothesis for Synapsin function is that the type I adenylate cyclase (coding gene: rut, CG9533) detects a coincidence of odor-induced activity in mushroom body neurons on the one hand, and of an internal aminergic reinforcement signal on the other hand, such that the cAMP-PKA cascade is activated in an odor-specific subset of mushroom body neurons (Tomchik and Davis 2009;Gervasi et al 2010). Arguably, Synapsin is one of the target proteins of PKA (Fiumara et al 2004;Michels et al 2011) such that upon phosphorylation of Synapsin its affinity to the cytoskeleton is reduced and reserve-pool vesicles can be recruited. Thus, when the trained odor is encountered thereafter, more synaptic vesicles will be available for release (Shupliakov et al 2011).…”

mentioning

confidence: 99%

See 2 more Smart Citations

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

et al. 2015

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Neuropeptide F neurons modulate sugar reward during associative olfactory learning of Drosophila larvae

Rohwedder

Selcho

Chassot

et al. 2015

J of Comparative Neurology

View full text Add to dashboard Cite

All organisms continuously have to adapt their behavior according to changes in the environment in order to survive. Experience-driven changes in behavior are usually mediated and maintained by modifications in signaling within defined brain circuits. Given the simplicity of the larval brain of Drosophila and its experimental accessibility on the genetic and behavioral level, we analyzed if Drosophila neuropeptide F (dNPF) neurons are involved in classical olfactory conditioning. dNPF is an ortholog of the mammalian neuropeptide Y, a highly conserved neuromodulator that stimulates food-seeking behavior. We provide a comprehensive anatomical analysis of the dNPF neurons on the single-cell level. We demonstrate that artificial activation of dNPF neurons inhibits appetitive olfactory learning by modulating the sugar reward signal during acquisition. No effect is detectable for the retrieval of an established appetitive olfactory memory. The modulatory effect is based on the joint action of three distinct cell types that, if tested on the single-cell level, inhibit and invert the conditioned behavior. Taken together, our work describes anatomically and functionally a new part of the sugar reinforcement signaling pathway for classical olfactory conditioning in Drosophila larvae.

show abstract

Cellular site and molecular mode of synapsin action in associative learning

Cited by 49 publications

References 81 publications

Olfactory memories are intensity specific in larval Drosophila

Olfactory memories are intensity specific in larval Drosophila

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

Neuropeptide F neurons modulate sugar reward during associative olfactory learning of Drosophila larvae

Contact Info

Product

Resources

About