Parametric and genetic analysis of <i>Drosophila </i>appetitive long‐term memory and sugar motivation

Colomb, Julien; Kaiser, Laure; Chabaud, Marie-Ange; Préat, Thomas

doi:10.1111/j.1601-183x.2009.00482.x

Cited by 101 publications

(127 citation statements)

References 33 publications

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“…For example, crammer mutant flies were reported to either show 12 or not show 13 an appetitive short term memory deficit with identical memory retention scores, because the scores of the control “CS” flies were different in the two studies. Our results further emphasize the need for a more systematic scheme addressing control populations.…”

Section: Discussionmentioning

confidence: 99%

Sub-strains of Drosophila Canton-S differ markedly in their locomotor behavior

Colomb

Brembs

2014

F1000Res

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We collected five sub-strains of the standard laboratory wild-type Drosophila melanogaster Canton Special (CS) and analyzed their walking behavior in Buridan's paradigm using the CeTrAn software. According to twelve different aspects of their behavior, the sub-strains fit into three groups. The group separation appeared not to be correlated with the origin of the stocks. We conclude that founder effects but not laboratory selection likely influenced the gene pool of the sub-strains. The flies’ stripe fixation was the parameter that varied most. Our results suggest that differences in the genome of laboratory stocks can render comparisons between nominally identical wild-type stocks meaningless. A single source for control strains may settle this problem.

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Section: Discussionmentioning

confidence: 99%

Sub-strains of Drosophila Canton-S differ markedly in their locomotor behavior

Colomb

Brembs

2014

F1000Res

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“…In order to determine whether MB-V2 output is required for all types of memory retrieval, we performed appetitive conditioning, where electric shocks are replaced by sugar reward 24 . A sugar response defect was observed in NP2492/UAS-shi ts flies tested at restrictive temperature ( Supplementary Fig.…”

Section: Mb-v2 Output Is Required For Olfactory Memory Retrievalmentioning

confidence: 99%

“…A performance index (PI) results from the average of two reciprocal experiments. For appetitive training, electric shocks were replaced by 1-minute sugar exposure, as previously described 24 .…”

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confidence: 99%

Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Séjourné¹,

Plaçais²,

et al. 2011

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6 These authors contributed equally to this work. 2 Aversive olfactory memory is formed in the Drosophila mushroom bodies (MB).Memory retrieval requires MB output, but it remains unknown how a memory trace in the MB drives conditioned avoidance of a learned odour. To identify neurons involved in olfactory memory retrieval, we performed an anatomical and functional screen of defined sets of MB extrinsic neurons. Here we show that MB-V2 neurons are essential for retrieval of both short-and long-lasting memory, but neither for memory formation nor for memory consolidation. We further show that MB-V2 are cholinergic efferent neurons that project from the MB vertical lobes to the middle superiormedial protocerebrum and the lateral horn (LH). Notably, the odour response of MB-V2 neurons is modified after conditioning. As the LH is implicated in innate responses to repellent odorants, we propose that during memory retrieval, MB-V2 neurons reinforce the olfactory pathway involved in innate odour avoidance.Different odours induce innate approach or avoidance behaviours in Drosophila. Innate odour responses can be modulated by experience, such as associative learning. After simultaneous exposure to an electric shock and an odorant, flies form aversive memory and show robust conditioned odour avoidance that lasts for hours to days, depending on the training protocol [1][2][3] . The neural pathways for odour or shock processing and signal integration in the fly brain have been intensely studied in recent years. Odour information is first represented in the antennal lobes in the form of olfactory receptor neuron activity 4 . Projection neurons then convey this information to higher order processing centres 4 : the mushroom bodies (MB) and the lateral horn (LH). In contrast, aversive reinforcement signals in response to electric shock are relayed to the MB via dopaminergic neurons [5][6][7] . The olfactory and 3 electric shock signals are integrated in the MB to form aversive olfactory memory 1, 2 . The MB are however dispensable for innate avoidance of the repellent odours 8,9 .In adult Drosophila, the MB consist of approximately 2000 Kenyon cells per brain hemisphere, which may be classified into three major types based on their axonal projection: γ neurons, which form only a medial lobe, α/β neurons, whose axons branch to form a vertical (α) and a medial (β) lobe, and α'/β' neurons, which also form a vertical (α') and a medial (β') lobe 10 . Functional brain imaging has revealed localised activation of cAMP/PKA signalling in the MB α lobe in response to simultaneous cholinergic and dopaminergic stimulation 11,12 , that represent respectively the odorant and electric shock pathways.Following associative conditioning, calcium imaging studies have shown that a short-term memory trace is formed in the α'/β' neurons 13, and a long-term one in α lobes 14 . Previous studies have shown that the output of the α/β neurons is necessary for the retrieval of all phases of olfactory memory 15,16 , but the neural circuits that translate ...

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“…Whereas some forms of long-term memory (LTM) require repetitive training (1-3), a highly relevant stimulus such as food or poison is sufficient to induce LTM in a single training session (4)(5)(6)(7). Recent studies have revealed aspects of the molecular and cellular mechanisms of LTM formation induced by repetitive training (8)(9)(10)(11), but how a single training induces a stable LTM is poorly understood (12).…”

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confidence: 99%

“…Appetitive olfactory learning in fruit flies is suited to address the question, as a presentation of a sugar reward paired with odor induces robust short-term memory (STM) and LTM (6,7). Odor is represented by a sparse ensemble of the 2,000 intrinsic neurons, the Kenyon cells (13).…”

mentioning

confidence: 99%

Distinct dopamine neurons mediate reward signals for short- and long-term memories

Yamagata

Ichinose

Aso

et al. 2014

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

238

287

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Drosophila melanogaster can acquire a stable appetitive olfactory memory when the presentation of a sugar reward and an odor are paired. However, the neuronal mechanisms by which a single training induces long-term memory are poorly understood. Here we show that two distinct subsets of dopamine neurons in the fly brain signal reward for short-term (STM) and long-term memories (LTM). One subset induces memory that decays within several hours, whereas the other induces memory that gradually develops after training. They convey reward signals to spatially segregated synaptic domains of the mushroom body (MB), a potential site for convergence. Furthermore, we identified a single type of dopamine neuron that conveys the reward signal to restricted subdomains of the mushroom body lobes and induces long-term memory. Constant appetitive memory retention after a single training session thus comprises two memory components triggered by distinct dopamine neurons.dopamine | learning and memory | Drosophila | mushroom body M emory of a momentous event persists for a long time.Whereas some forms of long-term memory (LTM) require repetitive training (1-3), a highly relevant stimulus such as food or poison is sufficient to induce LTM in a single training session (4-7). Recent studies have revealed aspects of the molecular and cellular mechanisms of LTM formation induced by repetitive training (8-11), but how a single training induces a stable LTM is poorly understood (12).Appetitive olfactory learning in fruit flies is suited to address the question, as a presentation of a sugar reward paired with odor induces robust short-term memory (STM) and LTM (6, 7). Odor is represented by a sparse ensemble of the 2,000 intrinsic neurons, the Kenyon cells (13). A current working model suggests that concomitant reward signals from sugar ingestion cause associative plasticity in Kenyon cells that might underlie memory formation (14-20). A single activation session of a specific cluster of dopamine neurons (PAM neurons) by sugar ingestion can induce appetitive memory that is stable over 24 h (19), underscoring the importance of sugar reward to the fly.The mushroom body (MB) is composed of the three different cell types, α/β, α′/β′, and γ, which have distinct roles in different phases of appetitive memories (11,(21)(22)(23)(24)(25). Similar to midbrain dopamine neurons in mammals (26,27), the structure and function of PAM cluster neurons are heterogeneous, and distinct dopamine neurons intersect unique segments of the MB lobes (19,(28)(29)(30)(31)(32)(33)(34). Further circuit dissection is thus crucial to identify candidate synapses that undergo associative modulation.By activating distinct subsets of PAM neurons for reward signaling, we found that short-and long-term memories are independently formed by two complementary subsets of PAM cluster dopamine neurons. Conditioning flies with nutritious and nonnutritious sugars revealed that the two subsets could represent different reinforcing properties: sweet taste and nutritional value of sugar....

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Parametric and genetic analysis of Drosophila appetitive long‐term memory and sugar motivation

Cited by 101 publications

References 33 publications

Sub-strains of Drosophila Canton-S differ markedly in their locomotor behavior

Sub-strains of Drosophila Canton-S differ markedly in their locomotor behavior

Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila

Distinct dopamine neurons mediate reward signals for short- and long-term memories

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