Reversing Stimulus Timing in Visual Conditioning Leads to Memories with Opposite Valence in Drosophila

Vogt, Katrin; Yarali, Ayse; Tanimoto, Hiromu

doi:10.1371/journal.pone.0139797

Cited by 28 publications

(25 citation statements)

References 39 publications

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“…Behavioral responses shaped by relief learning appear to be of weaker strength (Tanimoto et al, 2004; Gerber et al, 2014; Vogt et al, 2015), which corresponds well with our own findings. However, it is important to note that our paradigm differed from the previous studies on relief-learning in Drosophila , most notably in that it contained an operant element (shocks could be avoided).…”

Section: Discussionsupporting

confidence: 90%

Aversive Learning of Colored Lights in Walking Honeybees

Kirkerud

Schlegel

Galizia

2017

Front. Behav. Neurosci.

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The honeybee has been established as an important model organism in studies on visual learning. So far the emphasis has been on appetitive conditioning, simulating floral discrimination, and homing behavior, where bees perform exceptionally well in visual discrimination tasks. However, bees in the wild also face dangers, and recent findings suggest that what is learned about visual percepts is highly context dependent. A stimulus that follows an unpleasant period, is associated with the feeling of relief- or safety in humans and animals, thus acquiring a positive meaning. Whether this is also the case in honeybees is still an open question. Here, we conditioned bees aversively in a walking arena where each half was illuminated by light of a specific wavelength and intensity, one of which was combined with electric shocks. In this paradigm, the bees' preferences to the different lights were modified through nine conditioning trials, forming robust escape, and avoidance behaviors. Strikingly, we found that while 465 nm (human blue) and 590 nm (human yellow) lights both could acquire negative valences (inducing avoidance response), 525 nm (human green) light could not. This indicates that green light holds an innate meaning of safety which is difficult to overrule even through intensive aversive conditioning. The bees had slight initial preferences to green over the blue and the yellow lights, which could be compensated by adjusting light intensity. However, this initial bias played a minor role while the chromatic properties were the most salient characteristics of the light stimuli during aversive conditioning. Moreover, bees could learn the light signaling safety, revealing the existence of a relief component in aversive operant conditioning, similar to what has been observed in other animals.

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Section: Discussionsupporting

confidence: 90%

Aversive Learning of Colored Lights in Walking Honeybees

Kirkerud

Schlegel

Galizia

2017

Front. Behav. Neurosci.

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“…In this work, this definition will be used to refer to an appetitive experience. These kind of aversive and relief memories could be found in phylogenetically distant species such as fly, rats, mice and humans (Andreatta et al, 2012; Vogt et al, 2015). …”

Section: Introductionmentioning

confidence: 99%

Requirement of NF-kappa B Activation in Different Mice Brain Areas during Long-Term Memory Consolidation in Two Contextual One-Trial Tasks with Opposing Valences

Salles

Krawczyk

Blake

et al. 2017

Front. Mol. Neurosci.

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NF-kappa B is a transcription factor whose activation has been shown to be necessary for long-term memory consolidation in several species. NF-kappa B is activated and translocates to the nucleus of cells in a specific temporal window during consolidation. Our work focuses on a one trial learning tasks associated to the inhibitory avoidance (IA) setting. Mice were trained either receiving or not a footshock when entering a dark compartment (aversive vs. appetitive learning). Regardless of training condition (appetitive or aversive), latencies to step-through during testing were significantly different to those measured during training. Additionally, these testing latencies were also different from those of a control group that only received a shock unrelated to context. Moreover, nuclear NF-kappa B DNA-binding activity was augmented in the aversive and the appetitive tasks when compared with control and naïve animals. NF-kappa B inhibition by Sulfasalazine injected either in the Hippocampus, Amygdala or Nucleus accumbens immediately after training was able to impair retention in both training versions. Our results suggest that NF-kappa B is a critical molecular step, in different brain areas on memory consolidation. This was the case for both the IA task and also the modified version of the same task where the footshock was omitted during training. This work aims to further investigate how appetitive and aversive memories are consolidated.

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“…Punishment-memory scores were dramatically stronger than relief-memory scores, as was the case in all previous datasets directly comparing these two kinds of memory in the fruit fly [2–8] (see [12] for a meta-analysis). Indeed, among the 38 inbred strains tested, all showed significant punishment-memory, except one strain with a tendency only for punishment-memory; whereas six strains had significant relief-memory, with nine further strains showing a tendency towards it (figure 2 a , one-sided one-sample Wilcoxon signed-rank tests using a false discovery rate less than 0.05 for significance criterion and p < 0.05 for tendency criterion; see electronic supplementary material, table S1 for data and statistical report).…”

Section: Resultsmentioning

confidence: 76%

Independent natural genetic variation of punishment- versus relief-memory

et al. 2016

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A painful event establishes two opponent memories: cues that are associated with pain onset are remembered negatively, whereas cues that coincide with the relief at pain offset acquire positive valence. Such punishment- versus relief-memories are conserved across species, including humans, and the balance between them is critical for adaptive behaviour with respect to pain and trauma. In the fruit fly, Drosophila melanogaster as a study case, we found that both punishment- and relief-memories display natural variation across wild-derived inbred strains, but they do not covary, suggesting a considerable level of dissociation in their genetic effectors. This provokes the question whether there may be heritable inter-individual differences in the balance between these opponent memories in man, with potential psycho-clinical implications.

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Reversing Stimulus Timing in Visual Conditioning Leads to Memories with Opposite Valence in Drosophila

Cited by 28 publications

References 39 publications

Aversive Learning of Colored Lights in Walking Honeybees

Aversive Learning of Colored Lights in Walking Honeybees

Requirement of NF-kappa B Activation in Different Mice Brain Areas during Long-Term Memory Consolidation in Two Contextual One-Trial Tasks with Opposing Valences

Independent natural genetic variation of punishment- versus relief-memory

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