Memory decay and susceptibility to amnesia dissociate punishment- from relief-learning

Diegelmann, Soeren; Preuschoff, Stephan; Appel, Mirjam; Niewalda, Thomas; Gerber, Bertram; Yarali, Ayse

doi:10.1098/rsbl.2012.1171

Cited by 10 publications

(32 citation statements)

References 14 publications

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“…Do our results support this hypothesis? If the CS turns into a predictor for punishment, i.e., an aversive situation, we would expect withholding of the response when the CS is presented (Smith et al 1991;Diegelmann et al 2013). We observed withholding of the odor response 30 min after backward conditioning.…”

Section: 'Punishment Learning' During Backward Conditioning With a Rementioning

confidence: 57%

Short- and long-term memories formed upon backward conditioning in honeybees (Apis mellifera)

et al. 2014

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In classical conditioning, the temporal sequence of stimulus presentations is critical for the association between the conditioned stimulus (CS) and the unconditioned stimulus (US). In forward conditioning, the CS precedes the US and is learned as a predictor for the US. Thus it acquires properties to elicit a behavioral response, defined as excitatory properties. In backward conditioning, the US precedes the CS. The CS might be learned as a predictor for the cessation of the US acquiring inhibitory properties that inhibit a behavioral response. Interestingly, behavior after backward conditioning is controlled by both excitatory and inhibitory properties of the CS, but the underlying mechanisms determining which of these opposing properties control behavior upon retrieval is poorly understood. We performed conditioning experiments in the honeybee (Apis mellifera) to investigate the CS properties that control behavior at different time points after backward conditioning. The CS properties, as characterized by the retardation or enhancement of subsequent acquisition, were examined 30 min and 24 h after backward conditioning. We found that 30 min after backward conditioning, the CS acquired an inhibitory property during backward conditioning depending on the intertrial interval, the number of trials, and the odor used as the CS. One day after backward conditioning, we observed significant retardation of acquisition. In addition, we demonstrated an enhanced, generalized odor response in the backward conditioned group compared to untreated animals. These results indicate that two long-lasting opposing memories have been formed in parallel: one about the excitatory properties of the CS and one about the inhibitory properties of the CS.

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Section: 'Punishment Learning' During Backward Conditioning With a Rementioning

confidence: 57%

Short- and long-term memories formed upon backward conditioning in honeybees (Apis mellifera)

et al. 2014

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“…Interestingly, in wild-type flies an application of cold shock between training and test induces a partial amnesia of punishment memory, and the residual amnesia-resistant memory does not require Synapsin (Knapek et al, 2010). Given that relief memory is fully abolished upon loss of function of Synapsin, one would thus reason that cold shock should fully abolish relief memoryand intriguingly this is what Diegelmann et al (2013b) have found. The emerging scenario is that punishment learning establishes two short-term memory components: one that is Synapsin dependent and amnesia sensitive, and one that is Synapsin independent and amnesia resistant.…”

Section: Discussionmentioning

confidence: 89%

“…Given the 28 phosphorylated sites of Synapsin, targeted by up to 11 different kinases (Fig. 2, Table 1; Michels et al, 2011;Nuwal et al, 2011;Sadanandappa et al, 2013;Diegelmann et al, 2013a), it is conceivable that different kinases and/or phosphorylation sites of the Synapsin protein could be used during relief learning and punishment learning. Likewise, the mRNA editing observed for one of the phosphorylation sites of Synapsin (Diegelmann et al, 2006) could be selectively involved in relief learning and punishment learning, in particular as the proteins corresponding to both the edited and the nonedited version are indeed expressed (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…In this sense, Synapsin is thought to function during learning in a way that determines memory strength. It contributes to the regulation of synaptic output and various forms of memory throughout the animal kingdom (Silva et al, 1996;Hilfiker et al, 1999;Garcia et al, 2004;Gitler et al, 2004;Südhof, 2004;Greco et al, 2013;Diegelmann et al, 2013a;Sadanandappa et al, 2013;Vasin et al, 2014). Regarding associative processing in Drosophila, Synapsin null mutants show reduced scores in onetrial strong-shock punishment memory, reduced spatial memory in the heat-box paradigm and, as larvae, reduced odor- Figure 2.…”

Section: Introductionmentioning

confidence: 99%

“…We chose the Synapsin protein as a study case (coded by the synapsin gene: CG3985), a ubiquitously and abundantly expressed, and evolutionarily conserved, presynaptic phosphoprotein (Klagges et al, 1996;Nuwal et al, 2011;Diegelmann et al, 2013a). It can tether reserve-pool vesicles to the cytoskeleton and, during learning, regulate their recruitment to the readily releasable pool in a phosphorylation-dependent way.…”

Section: Introductionmentioning

confidence: 99%

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Synapsin Determines Memory Strength after Punishment- and Relief-Learning

et al. 2015

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Adverse life events can induce two kinds of memory with opposite valence, dependent on timing: "negative" memories for stimuli preceding them and "positive" memories for stimuli experienced at the moment of "relief." Such punishment memory and relief memory are found in insects, rats, and man. For example, fruit flies (Drosophila melanogaster) avoid an odor after odor-shock training ("forward conditioning" of the odor), whereas after shock-odor training ("backward conditioning" of the odor) they approach it. Do these timingdependent associative processes share molecular determinants? We focus on the role of Synapsin, a conserved presynaptic phosphoprotein regulating the balance between the reserve pool and the readily releasable pool of synaptic vesicles. We find that a lack of Synapsin leaves task-relevant sensory and motor faculties unaffected. In contrast, both punishment memory and relief memory scores are reduced. These defects reflect a true lessening of associative memory strength, as distortions in nonassociative processing (e.g., susceptibility to handling, adaptation, habituation, sensitization), discrimination ability, and changes in the time course of coincidence detection can be ruled out as alternative explanations. Reductions in punishment-and relief-memory strength are also observed upon an RNAi-mediated knock-down of Synapsin, and are rescued both by acutely restoring Synapsin and by locally restoring it in the mushroom bodies of mutant flies. Thus, both punishment memory and relief memory require the Synapsin protein and in this sense share genetic and molecular determinants. We note that corresponding molecular commonalities between punishment memory and relief memory in humans would constrain pharmacological attempts to selectively interfere with excessive associative punishment memories, e.g., after traumatic experiences.

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Aversive teaching signals from individual dopamine neurons in larval Drosophila show qualitative differences in their temporal “fingerprint”

Weiglein

Thoener

Feldbruegge

et al. 2021

J of Comparative Neurology

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Dopamine serves many functions, and dopamine neurons are correspondingly diverse. We use a combination of optogenetics, behavioral experiments, and high-resolution videotracking to probe for the functional capacities of two single, identified dopamine neurons in larval Drosophila. The DAN-f1 and the DAN-d1 neuron were recently found to carry aversive teaching signals during Pavlovian olfactory learning. We enquire into a fundamental feature of these teaching signals, namely their temporal "fingerprint". That is, receiving punishment feels bad, whereas being relieved from it feels good, and animals and humans alike learn with opposite valence about the occurrence and the termination of punishment (the same principle applies in the appetitive domain, with opposite sign). We find that DAN-f1 but not DAN-d1 can mediate such timing-dependent valence reversal: presenting an odor before DAN-f1 activation leads to learned avoidance of the odor (punishment memory), whereas presenting the odor upon termination of DAN-f1 activation leads to learned approach (relief memory). In contrast, DAN-d1 confers punishment memory only. These effects are further characterized in terms of the impact of the duration of optogenetic activation, the temporal stability of the memories thus established, and the specific microbehavioral patterns of locomotion through which they are expressed. Together with recent findings in the appetitive domain and from adult Drosophila, our results suggest that heterogeneity in the temporal fingerprint of teaching signals might be a more general principle of reinforcement processing through dopamine neurons.

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Memory decay and susceptibility to amnesia dissociate punishment- from relief-learning

Cited by 10 publications

References 14 publications

Short- and long-term memories formed upon backward conditioning in honeybees (Apis mellifera)

Short- and long-term memories formed upon backward conditioning in honeybees (Apis mellifera)

Synapsin Determines Memory Strength after Punishment- and Relief-Learning

Aversive teaching signals from individual dopamine neurons in larval Drosophila show qualitative differences in their temporal “fingerprint”

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