Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila

Aso, Yoshinori; Sitaraman, Divya; Ichinose, Toshiharu; Kaun, Karla R.; Vogt, Katrin; Belliart-Guérin, Ghislain; Plaçais, Pierre Yves; Robie, Alice A.; Yamagata, Nobuhiro; Schnaitmann, Christopher; Rowell, William J; Johnston, Rebecca M.; Ngo, Teri T.B.; Chen, Nan; Korff, Wyatt; Nitabach, Michael N.; Heberlein, Ulrike; Préat, Thomas; Branson, Kristin; Tanimoto, Hiromu; Rubin, Gerald M.

doi:10.7554/elife.04580

Cited by 649 publications

(1,076 citation statements)

References 149 publications

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“…We next sought to identify individual reward neurons by examining the correlation between induced memory performances and GAL4 expression in all cell types of PAM cluster neurons. To this end, we used a collection of 20 Split-GAL4 driver lines with specific expression in different PAM cluster neurons; the construction and detailed anatomical analysis of these lines are described in Aso et al (33,34). We performed a behavioral screen of thermoactivation in starved flies with this driver collection and measured the formation of STM and LTM.…”

Section: Prediction Of Individual Dopamine Neurons For Ltm Formation Bymentioning

confidence: 99%

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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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Section: Prediction Of Individual Dopamine Neurons For Ltm Formation Bymentioning

confidence: 99%

“…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.…”

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.

Self Cite

238

287

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“…For example, spGAL4 combinations have been identified that express in the different neurons innervating the fly mushroom body (Aso et al 2014a) and visual system (Tuthill et al 2013;Nern et al 2015). The activity of each neuron type was then systematically manipulated to assess their contributions to different behaviors (Tuthill et al 2013;Aso et al 2014b). Such approaches facilitate the systematic dissection of neurons that make up specific brain regions, and the assessment of their contributions to behavior.…”

Section: Complementary Approachesmentioning

confidence: 99%

“…Systems have also been developed that direct laser pulses to specific body parts of a moving fly . Other systems restrict light to particular regions of a chamber allowing flies to "choose" whether the neurons are activated (or not) by moving into (or out of) the illuminated region, or coupling neural activation with particular localized features of a larger chamber, such as odors (Suh et al 2007;Lin et al 2013a;Aso et al 2014b;Klapoetke et al 2014;Lin et al 2015).…”

Section: Hardware For Thermo-and Optogenetic Behavioral Experimentsmentioning

confidence: 99%

“…This has revealed how neurons can elicit persistent behaviors or cause alterations in behavioral states (Inagaki et al 2014;Bath et al 2014;Hoopfer et al 2015;Hampel et al 2015). Different odorant or food conditions have been used to study their contributions to feeding, attraction, avoidance, social behaviors, and learning (Gao et al 2013;Aso et al 2014b;Lim et al 2014;Ramdya et al 2014;Albin et al 2015). Wild type, mutant, and flies with neural manipulations have been used to test different cues of conspecific flies that can affect social behaviors Hoopfer et al 2015).…”

Section: Annotating Behaviors Elicited By Neural Manipulationsmentioning

confidence: 99%

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Targeted manipulation of neuronal activity in behaving adult flies

Hampel

Seeds

2016

Preprint

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The ability to control the activity of specific neurons in freely behaving animals provides an effective way to probe the contributions of neural circuits to behavior. Wide interest in studying principles of neural circuit function using the fruit fly Drosophila melanogaster has fueled the construction of an extensive transgenic toolkit for performing such neural manipulations. Here we describe approaches for using these tools to manipulate the activity of specific neurons and assess how those manipulations impact the behavior of flies. We also describe methods for examining connectivity among multiple neurons that together form a neural circuit controlling a specific behavior. This work provides a resource ABSTRACTThe ability to control the activity of specific neurons in freely behaving animals provides an effective way to probe the contributions of neural circuits to behavior. Wide interest in studying principles of neural circuit function using the fruit fly Drosophila melanogaster has fueled the construction of an extensive transgenic toolkit for performing such neural manipulations. Here we describe approaches for using these tools to manipulate the activity of specific neurons and assess how those manipulations impact the behavior of flies. We also describe methods for examining connectivity among multiple neurons that together form a neural circuit controlling a specific behavior. This work provides a resource for researchers interested in examining how neurons and neural circuits contribute to the rich repertoire of behaviors performed by flies.

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Suppression of a single pair of mushroom body output neurons in Drosophila triggers aversive associations

et al. 2017

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Memory includes the processes of acquisition, consolidation and retrieval. In the study of aversive olfactory memory in Drosophila melanogaster, flies are first exposed to an odor (conditioned stimulus, CS+) that is associated with an electric shock (unconditioned stimulus, US), then to another odor (CS−) without the US, before allowing the flies to choose to avoid one of the two odors. The center for memory formation is the mushroom body which consists of Kenyon cells (KCs), dopaminergic neurons (DANs) and mushroom body output neurons (MBONs). However, the roles of individual neurons are not fully understood. We focused on the role of a single pair of GABAergic neurons (MBON‐γ1pedc) and found that it could inhibit the effects of DANs, resulting in the suppression of aversive memory acquisition during the CS− odor presentation, but not during the CS+ odor presentation. We propose that MBON‐γ1pedc suppresses the DAN‐dependent effect that can convey the aversive US during the CS− odor presentation, and thereby prevents an insignificant stimulus from becoming an aversive US.

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Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila

Cited by 649 publications

References 149 publications

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

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

Targeted manipulation of neuronal activity in behaving adult flies

Suppression of a single pair of mushroom body output neurons in Drosophila triggers aversive associations

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