Distinct Dopamine Receptor Pathways Underlie the Temporal Sensitivity of Associative Learning

Handler, Annie; Graham, Thomas G.W.; Cohn, Raphael; Morantte, Ianessa; Siliciano, Andrew F.; Zeng, Jianzhi; Li, Yulong; Ruta, Vanessa

doi:10.1016/j.cell.2019.05.040

Cited by 203 publications

(328 citation statements)

References 95 publications

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“…Recent studies have modeled networks with other forms of differentiable plasticity, including Hebbian plasticity (Ba et al, 2016;Miconi et al, 2018;Orhan and Ma, 2019). In our case, detailed knowledge of the site and functional form of plasticity (Handler et al, 2019) allowed us to investigate specific predictions about DAN responses. Similar approaches may be effective for modeling other brain areas in which the neurons responsible for conveying "error" signals can be identified, such as the cerebellum or basal ganglia (Ito et al, 1982;Watabe-Uchida et al, 2017).…”

Section: Relationship To Other Modeling Approachesmentioning

confidence: 92%

“…1A) (Handler et al, 2019). We modeled this plasticity by assuming that each element w of W KC→MBON is a dynamic quantity that is modified according to the following update rule: (Handler et al, 2019). The seconds-long timescale of this curve is compatible with the use of continuous firing rates rather than discrete spike timing to model KC-to-MBON plasticity, as we have done in Eq.…”

Section: Modeling Recurrent Mushroom Body Output Circuitrymentioning

confidence: 99%

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Models of heterogeneous dopamine signaling in an insect learning and memory center

Jiang

Litwin-Kumar

2019

Preprint

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The Drosophila mushroom body exhibits dopamine (DA) dependent synaptic plasticity that underlies the acquisition and retrieval of associative memories. Classic studies have recorded DA activity in this system and identified signals related to external reinforcement such as reward and punishment. However, recent studies have found that other factors including locomotion, novelty, reward expectation, and internal state also modulate DA neurons. This heterogeneous activity is at odds with typical modeling approaches in which DA neurons are assumed to encode a global, scalar error signal. How can DA signals support appropriate synaptic plasticity in the presence of this heterogeneity? We develop a modeling approach that infers a pattern of DA activity that is sufficient to solve a defined set of behavioral tasks, given architectural constraints informed by knowledge of mushroom body circuitry. Model DA neurons exhibit diverse tuning to task parameters while nonetheless producing coherent learned behaviors. Our results provide a mechanistic framework that accounts for the heterogeneity of DA signals observed during learning and behavior.

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Section: Relationship To Other Modeling Approachesmentioning

confidence: 92%

Section: Modeling Recurrent Mushroom Body Output Circuitrymentioning

confidence: 99%

Models of heterogeneous dopamine signaling in an insect learning and memory center

Jiang

Litwin-Kumar

2019

Preprint

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“…Interestingly, some MBONs receive input from both the taste (β'2) and nutrient (γ5) compartments, raising the possibility that sensory and nutrient memories may be integrated in the same cells to regulate different aspects of the satiety cascade (satiation vs. satiety). In flies, the mode and timing of DA delivery onto the MBONs is critical to establish the strength and valence of the associations(Handler et al 2019) .…”

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confidence: 99%

Dietary sugar inhibits satiation by decreasing the central processing of sweet taste

May

Rosander

Gottfried

et al. 2019

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From humans to flies, exposure to diets rich in sugar and fat lowers taste sensation, changes food choices, and promotes feeding. However, how these peripheral alterations influence eating is unknown. Here we used the genetically tractable organism D. melanogaster to define the neural mechanisms through which this occurs. We characterized a population of protocerebral anterior medial dopaminergic neurons (PAM DANs) that innervates the β'2 compartment of the mushroom body and responds to sweet taste. In animals fed a high sugar diet, the response of PAM-β'2 to sweet stimuli was reduced and delayed, and sensitive to the strength of the signal transmission out of the sensory neurons. We found that PAM-β'2 DANs activity controls feeding rate and satiation: closed-loop optogenetic activation of β'2 DANs restored normal eating in animals fed high sucrose. These data argue that diet-dependent alterations in taste weaken satiation by impairing the central processing of sensory signals.

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“…The valence of olfactory memories can be reversed from aversive to appetitive by changing the relative timing of odor and reinforcement presentation during training (Tanimoto et al, 2004;König et al, 2018). If shock, or artificial DAN activation is presented <45 seconds before odor presentation flies form an appetitive 'relief memory' for that odor (Tanimoto et al, 2004;Aso and Rubin, 2016;Handler et al, 2019). Experiments with artificial DAN activation suggest that relief learning is represented by dopamine potentiating an MBONs response to the conditioned odor (Handler et al, 2019; although see König et al, 2018).…”

Section: Relief or Safety Memory?mentioning

confidence: 99%

“…If shock, or artificial DAN activation is presented <45 seconds before odor presentation flies form an appetitive 'relief memory' for that odor (Tanimoto et al, 2004;Aso and Rubin, 2016;Handler et al, 2019). Experiments with artificial DAN activation suggest that relief learning is represented by dopamine potentiating an MBONs response to the conditioned odor (Handler et al, 2019; although see König et al, 2018). If spaced training utilizes the same relief from punishment mechanism as that in Handler et al (2019), the CS-approach memory would be coded as potentiation of the same connections as those coding CS+ avoidance as a depression.…”

Section: Relief or Safety Memory?mentioning

confidence: 99%

Spaced training forms complementary long-term memories of opposite valence inDrosophila

Jacob

Waddell

2019

Preprint

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Forming long-term memory (LTM) in many cases requires repetitive experience spread over time. In Drosophila, aversive olfactory LTM is optimal following spaced training, multiple trials of differential odor conditioning with rest intervals. Studies often compare memory after spaced to that after massed training, same number of trials without interval. Here we show flies acquire additional information after spaced training, forming an aversive memory for the shock-paired odor and a 'safety-memory' for the explicitly unpaired odor. Safety-memory requires repetition, order and spacing of the training trials and relies on specific subsets of rewarding dopaminergic neurons. Co-existence of the aversive and safety memories can be measured as depression of odor-specific responses at different combinations of junctions in the mushroom body output network. Combining two particular outputs appears to signal relative safety. Learning a complementary safety memory thereby augments LTM performance after spaced training by making the odor preference more certain.

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Distinct Dopamine Receptor Pathways Underlie the Temporal Sensitivity of Associative Learning

Cited by 203 publications

References 95 publications

Models of heterogeneous dopamine signaling in an insect learning and memory center

Models of heterogeneous dopamine signaling in an insect learning and memory center

Dietary sugar inhibits satiation by decreasing the central processing of sweet taste

Spaced training forms complementary long-term memories of opposite valence inDrosophila

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