Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila

Plaçais, Pierre Yves; Trannoy, Séverine; Isabel, Guillaume; Aso, Yoshinori; Siwanowicz, Igor; Belliart-Guérin, Ghislain; Vernier, Philippe; Birman, Serge; Tanimoto, Hiromu; Préat, Thomas

doi:10.1038/nn.3055

Cited by 151 publications

(204 citation statements)

References 45 publications

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“…Lagasse et al, [40] selected flies bidirectionally for improved ARM or improved LTM, and found a functional and evolutionary trade-off between these two memory forms; flies with improved ARM had reduced LTM and vice versa. Interestingly, this finding correlates well with reports that ARM and LTM are mutually exclusive in flies; the formation of ARM prevents LTM consolidation and vice versa [41]. The dependency of LTM and ARM was also investigated by bidirectional artificial selection over nine generations in C. glomerata [42].…”

Section: Evolutionary Aspects Of Prepared Learningsupporting

confidence: 87%

“…In Drosophila, two pairs of dopaminergic neurons determine whether memory is gated into ARM or LTM, and these neurons are therefore candidates to play a role in the observed natural variation in this form of prepared learning [41]. Such a gating mechanism has so far only been found in Drosophila, and comparative studies of this mechanism on other species are complicated by fundamental differences in reward pathways between flies, honeybees and crickets.…”

Section: Mechanisms Underlying Natural Variation In Learning and Memorymentioning

confidence: 99%

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The complexity of learning, memory and neural processes in an evolutionary ecological context

Smid

Vet

2016

Current Opinion in Insect Science

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The ability to learn and form memories is widespread among insects, but there exists considerable natural variation between species and populations in these traits. Variation manifests itself in the way information is stored in different memory forms. This review focuses on ecological factors such as environmental information, spatial aspects of foraging behavior and resource distribution that drive the evolution of this natural variation and discusses the role of different genes and neural networks. We conclude that at the level of individual, population or species, insect learning and memory cannot be described as good or bad. Rather, we argue that insects evolve tailor-made learning and memory types; they gate learned information into memories with high or low persistence. This way, they are prepared to learn and form memory to optimally deal with the specific ecologies of their foraging environments. Highlights:• Environmental variation, spatial foraging behavior and the distribution of resources are factors that drive the evolution of differences in prepared learning • Considerable heritable variation exists in numerous learning and memory traits • Insects have evolved tailor-made memory types, adapted to the specific ecology of their foraging environment • The foraging gene is an important gene underlying natural variation in learning and memory • Dopaminergic signaling may drive the adaptive gating of information into different memory formsThe use of previous experience to optimize behavior in an adaptive manner is obviously of great benefit to all animals, including insects [1,2]. However, this does not mean that insects should learn and remember information from all possible experiences they encounter. Studies on diverse insect species have revealed the daunting complexity of different forms of memory each with different stabilities, including short-, mid-, anesthesia resistant-and long term memory (STM, MTM, ARM and LTM), e.g. [3][4][5][6]. In Fig. 1 we provide a basic description of these memory forms and their abbreviations. Why does learning not always result in the formation of LTM? To ensure the reliability of learned information, most animals require multiple, spaced experiences before information is stored as LTM. Nevertheless, some animals form LTM after a single experience suggesting that they may have evolved to rely on the Accepted in Current Opinion in Insect Science, CC-BY-NC-ND

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Section: Evolutionary Aspects Of Prepared Learningsupporting

confidence: 87%

Section: Mechanisms Underlying Natural Variation In Learning and Memorymentioning

confidence: 99%

The complexity of learning, memory and neural processes in an evolutionary ecological context

Smid

Vet

2016

Current Opinion in Insect Science

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“…4; regarding longer-term forms of memory and mechanisms of memory consolidation, see the recent studies by, e.g., Placais et al 2012or Perisse et al 2013 and references therein). Briefly, upon presentation of an odor, a particular combination of olfactory sensory neurons on the antennae and maxillary palps is activated according to the ligand profiles of the respectively expressed receptor proteins.…”

Section: Fly Punishment-and Reward-learningmentioning

confidence: 99%

“…Learning & Memory disentangle the specific roles for subsets of aminergic neurons, their target Kenyon cells, and the respectively expressed amine receptors in the acquisition, consolidation, or retrieval of various forms of olfactory memory as well as in motivational control of behavior (e.g., Krashes et al 2009;Berry et al 2012;Placais et al 2012;Perisse et al 2013; see also Burke et al 2012); for these aspects too, the roles of dopamine and octopamine apparently transgress the above-mentioned dichotomy. Thus, the striking valence-specificity of driving or impairing aminergic signaling seems to be a property of particular neurons and of their specific target receptors and cellular connectivity, rather than a property of transmitter systems as whole.…”

mentioning

confidence: 99%

Pain-relief learning in flies, rats, and man: basic research and applied perspectives

et al. 2014

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Memories relating to a painful, negative event are adaptive and can be stored for a lifetime to support preemptive avoidance, escape, or attack behavior. However, under unfavorable circumstances such memories can become overwhelmingly powerful. They may trigger excessively negative psychological states and uncontrollable avoidance of locations, objects, or social interactions. It is therefore obvious that any process to counteract such effects will be of value. In this context, we stress from a basic-research perspective that painful, negative events are "Janus-faced" in the sense that there are actually two aspects about them that are worth remembering: What made them happen and what made them cease. We review published findings from fruit flies, rats, and man showing that both aspects, respectively related to the onset and the offset of the negative event, induce distinct and oppositely valenced memories: Stimuli experienced before an electric shock acquire negative valence as they signal upcoming punishment, whereas stimuli experienced after an electric shock acquire positive valence because of their association with the relieving cessation of pain. We discuss how memories for such punishment-and relief-learning are organized, how this organization fits into the threat-imminence model of defensive behavior, and what perspectives these considerations offer for applied psychology in the context of trauma, panic, and nonsuicidal self-injury.The acknowledged "negative" mnemonic effects of adverse experiences mostly relate to what happens before the onset of an aversive, painful event. However, there is a less widely acknowledged type of memory that relates to what happens after the offset of or after escape from such a painful event, at the moment of "relief" (Fig. 1) (we use "relief" to refer specifically to the acute effects of punishment offset; an equally legitimate yet broader use of the word in, e.g., "fear relief," encompasses any process that eases fear [Riebe et al. 2012]). Indeed, in experimental settings, it turns out that stimuli experienced before and during a punishing episode are later avoided as they signal upcoming punishment, whereas stimuli experienced after a painful episode can subsequently prompt approach behavior, arguably (Box 1) because of their association with the relieving cessation of pain (Konorski 1948;Smith and Buchanan 1954;Wolpe and Lazarus 1966;Zanna et al. 1970;Solomon and Corbit 1974;Schull 1979;Solomon 1980;Wagner 1981;Walasek et al. 1995;Tanimoto et al. 2004;Yarali et al. 2008Yarali et al. , 2009bAndreatta et al. 2010Andreatta et al. , 2012Yarali and Gerber 2010;Ilango et al. 2012;Navratilova et al. 2012;Diegelmann et al. 2013b); for a corresponding finding in the appetitive domain, see Hellstern et al. (1998) andFelsenberg et al. (2013). Such relief can both support the learning of the cues associated with the disappearance of the threat and reinforce those behaviors that helped to escape it. Obviously, the positive conditioned valence of and ensuing learned approach behavi...

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“…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).…”

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.

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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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Slow oscillations in two pairs of dopaminergic neurons gate long-term memory formation in Drosophila

Cited by 151 publications

References 45 publications

The complexity of learning, memory and neural processes in an evolutionary ecological context

The complexity of learning, memory and neural processes in an evolutionary ecological context

Pain-relief learning in flies, rats, and man: basic research and applied perspectives

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

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