Drosophila Learn Opposing Components of a Compound Food Stimulus

Das, Gaurav; Klappenbach, Martín; Vrontou, Eleftheria; Perisse, Emmanuel; Clark, Christopher M.; Burke, Christopher J.; Waddell, Scott

doi:10.1016/j.cub.2014.05.078

Cited by 99 publications

(130 citation statements)

References 34 publications

(67 reference statements)

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“…Silencing only one of these dopaminergic neuron populations (MB058B) did not lead to disruption of the taste memory (Figure 2C and Figure S1A) suggesting that the collective action of these dopaminergic neurons may be required. Previous studies showed that PPL1-γ1pedc (MB-MP1) mediates the reinforcing property of electric shock and bitter taste for olfactory and visual learning [28, 35–37]. Interestingly, we found a strong impairment of taste memory by MB060B and MB065B, lines that broadly label PPL1 dopaminergic neurons but not the PPL1-γ1pedc (MB-MP1).…”

Section: Resultsmentioning

confidence: 48%

A Dopamine-Modulated Neural Circuit Regulating Aversive Taste Memory in Drosophila

et al. 2015

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Summary Taste memories allow animals to modulate feeding behavior in accordance with past experience and avoid the consumption of potentially harmful food [1]. We have developed a single-fly taste memory assay to functionally interrogate the neural circuitry encoding taste memories [2]. Here, we screen a collection of Split-GAL4 lines that label small populations of neurons associated with the fly memory center - the mushroom bodies (MB) [3]. Genetic silencing of PPL1 dopamine neurons disrupts conditioned, but not naïve feeding behavior, suggesting these neurons are selectively involved in the conditioned taste response. We identify two PPL1 subpopulations that innervate the MB α lobe and are essential for aversive taste memory. Thermogenetic activation of these dopamine neurons during training induces memory, indicating these neurons are sufficient for the reinforcing properties of bitter tastant to the MBs. Silencing of either the intrinsic MB neurons, or the output neurons from the α lobe, disrupts taste conditioning. Thermogenetic manipulation of these output neurons alters naïve feeding response, suggesting that dopamine neurons modulate the threshold of response to appetitive tastants. Taken together, these findings detail a neural mechanism underlying the formation of taste memory and provide a functional model for dopamine-dependent plasticity in Drosophila.

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Section: Resultsmentioning

confidence: 48%

A Dopamine-Modulated Neural Circuit Regulating Aversive Taste Memory in Drosophila

et al. 2015

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“…Strikingly, thermoactivation of the other subset of PAM cluster neurons with R15A04-GAL4 induced robust LTM without forming STM ( Fig. 1 H and I), similar to appetitive memory without a short-term component of mutants for TβH (36). The temporal dynamics of these two forms of memory were Significance A biologically relevant event such as finding food under starvation conditions or being poisoned can drive long-term memory (LTM) in a single training session.…”

Section: Resultsmentioning

confidence: 82%

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.

228

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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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“…In the T-maze used in flies to measure appetitive (30) and aversive memory (31), flies have to approach or avoid the arm containing the learned odor. When odors are associated with positive and negative rewards at the same time, the flies must decide between approaching or avoiding the odor, thus giving evidence of only one memory (17). In case of olfactory conditioning of proboscis extension in honey bees, the conditioned responses are either extending or withdrawing the proboscis upon stimulation with the odor (15,32).…”

Section: Discussionmentioning

confidence: 99%

“…However, if animals do not form any memory at all or if they form two opposite memories that compete during retrieval is not yet clear. A recent study in Drosophila indicates that appetitive and aversive memories are formed in parallel, and which memory prevails during memory expression depends on the time window in which memory is tested (17). Nevertheless, a limitation in these studies is that aversive and appetitive responses are mutually exclusive, which does not allow concluding whether the memory that is not observed does not exist or its expression is suppressed.…”

mentioning

confidence: 99%

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

Klappenbach

Nally

Locatelli

2017

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

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The neurobiology of learning and memory has been mainly studied by focusing on pure aversive or appetitive experiences. Here, we challenged this approach considering that real-life stimuli come normally associated with competing aversive and appetitive consequences and that interaction between conflicting information must be intrinsic part of the memory processes. We used Neohelice crabs, taking advantage of two well-described appetitive and aversive learning paradigms and combining them in a single training session to evaluate how this affects memory. We found that crabs build separate appetitive and aversive memories that compete during retrieval but not during acquisition. Which memory prevails depends on the balance between the strength of the unconditioned stimuli and on the motivational state of the animals. The results indicate that after a mix experience with appetitive and aversive consequences, parallel memories are established in a way that appetitive and aversive information is stored to be retrieved in an opportunistic manner.long-term memory | consolidation | retrieval | appetitive | aversive I n the wild, it is crucial for animals to learn and remember which places represent a danger and which ones are associated with appetitive rewards such as food, shelter, or mate. Understanding how these associations are acquired, retained, and retrieved are major goals in neurobiology. A successful strategy suited to laboratory conditions has been simplifying learning episodes to appetitive or aversive experiences, because in those ideal cases, learning and memory can be unequivocally measured as attraction or avoidance. The present study is framed on the view that those pure appetitive or aversive experiences do not fully represent real-life situations. In nature, animals are exposed to stimuli that predict positive and negative consequences at the same time, and the conflicting information must be weighed and organized to allow expression of the most beneficial behavior. Invertebrates are convenient models to study the interaction between appetitive and aversive memory processes because neurochemical pathways and circuits involved in both types of memory have begun to be elucidated (1-5). The hypothesis that appetitive and aversive information interact during memory processes gets support from pharmacological studies in crabs (6, 7) and bees (8,9), which show that the neurotransmitter necessary for appetitive memory formation does, in turn, impair aversive memory, whereas the transmitter necessary for aversive memory impairs appetitive memory. In addition, studies in Drosophila, in which memory mechanisms can be dissected at the neuron level, provide evidence that the interaction between appetitive and aversive information occurs from the circuits that encode reward and punishment to circuits that regulate memory expression (10)(11)(12)(13)(14).In contrast to the knowledge about the interaction at the circuit level, the description about the consequence of competing experiences in regards to the content of ...

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Drosophila Learn Opposing Components of a Compound Food Stimulus

Cited by 99 publications

References 34 publications

A Dopamine-Modulated Neural Circuit Regulating Aversive Taste Memory in Drosophila

A Dopamine-Modulated Neural Circuit Regulating Aversive Taste Memory in Drosophila

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

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

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