Independent Contributions of Discrete Dopaminergic Circuits to Cellular Plasticity, Memory Strength, and Valence in Drosophila

Boto, Tamara; Stahl, Aaron; Zhang, Xiaofan; Louis, Thierry; Tomchik, Seth M.

doi:10.1016/j.celrep.2019.04.069

Cited by 41 publications

(46 citation statements)

References 45 publications

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“…Interestingly, DANs respond to sensory stimuli including odors and temperature changes and 15 contribute to sensory valence decisions in naïve animals [18,25,[28][29][30][31][32]. Consistently, electron microscopic connectomics data from fly larvae and adults suggests that DANs, especially their axon terminals, receive odor information by KCs as part of a recurrent circuit [33][34][35] (Fig.…”

Section: Introductionmentioning

confidence: 76%

Valence and state-dependent population coding in dopaminergic neurons in the fly mushroom body

Siju

Štih

Aimon

et al. 2019

Preprint

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SummaryNeuromodulation permits flexibility of synapses, neural circuits and ultimately behavior. One neuromodulator, dopamine, has been studied extensively in its role as reward signal during learning and memory across animal species. Newer evidence suggests that dopaminergic neurons (DANs) can modulate sensory perception acutely, thereby allowing an animal to adapt its behavior and decision-making to its internal and behavioral state. In addition, some data indicate that DANs are heterogeneous and convey different types of information as a population. We have investigated DAN population activity and how it could encode relevant information about sensory stimuli and state by taking advantage of the confined anatomy of DANs innervating the mushroom body (MB) of the fly Drosophila melanogaster. Using in vivo calcium imaging and a custom 3D image registration method, we find that the activity of the population of MB DANs is predictive of the innate valence of an odor as well as the metabolic and mating state of the animal. Furthermore, DAN population activity is strongly correlated with walking or running, consistent with a role of dopamine in conveying behavioral state to the MB. Together our data and analysis suggest that distinct DAN population activities encode innate odor valence, movement and physiological state in a MB-compartment specific manner. We propose that dopamine shapes innate odor perception through combinatorial population coding of sensory valence, physiological and behavioral context.

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Section: Introductionmentioning

confidence: 76%

Valence and state-dependent population coding in dopaminergic neurons in the fly mushroom body

Siju

Štih

Aimon

et al. 2019

Preprint

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“…The Drosophila MB receives projections from different dopaminergic clusters to anatomically and functionally discrete compartments, whose output neurons direct different behaviors 43 . For example, the corner receives projections from PPL1 (projecting to γ1 and γ2) that control aversive olfactory learning, 6,44 and the medial tip receives projections from the PAM (projecting to γ3, γ4, and γ5) that control appetitive learning. 7,45 .…”

Section: Comparison Of Sex Differences In Evoked Dopamine Releasementioning

confidence: 99%

“…Protocerebral anterior medial (PAM) and protocerebral posterior lateral 2 (PPL2) neurons project to the tip of horizontal lobes and calyx, respectively, and PPL1 neurons project to the vertical lobes, heel, and peduncle of MB 5,6 . Each dopamine projection independently regulates synaptic activity in MB, promoting approach or avoidance behaviors, olfactory valence, and memory strength during olfactory learning 7,8 .…”

Section: Introductionmentioning

confidence: 99%

“…Each dopamine projection independently regulates synaptic activity in MB, promoting approach or avoidance behaviors, olfactory valence, and memory strength during olfactory learning 7,8 . Studies to investigate the dopaminergic system and underlying mechanism of learning and memory heavily rely on genetics, behavior assays, and calcium imaging [9][10][11] . These approaches reveal the function of specific genes, but lack the ability to monitor real-time changes of endogenous neurotransmission in Drosophila brains.…”

Section: Introductionmentioning

confidence: 99%

“…Oxidation current is normalized to the first stimulation for each experiment. Release is stable as there is no main effect of stimulation interval (Two-way ANOVA, F(1,8) = 0.3574, p=0.5665, n=5 each) or stimulation numbers (F(6,48) =0.6274, p=0.7075). * p<0.05, **p<0.01, ***p<0.001…”

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confidence: 98%

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Real-Time Measurement of Stimulated Dopamine Release in Compartments of the AdultDrosophila melanogasterMushroom Body

Shin

Copeland

Venton

2020

Preprint

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AbstractDrosophila melanogaster, the fruit fly, is an exquisite model organism to understand neurotransmission. Dopaminergic signaling in the Drosophila mushroom body (MB) is involved in olfactory learning and memory, with different compartments controlling aversive learning (corner) vs appetitive learning (medial tip). Here, the goal was to develop techniques to measure endogenous dopamine in compartments of the MB for the first time. We compared three stimulation methods: acetylcholine (natural stimulus), P2X2 (chemogenetics), and CsChrimson (optogenetics). Evoked dopamine release was measured with fast-scan cyclic voltammetry in isolated adult Drosophila brains. Acetylcholine stimulated the largest dopamine release (0.40 μM), followed by P2X2 (0.14 μM), and CsChrimson (0.07 μM). With the larger acetylcholine and P2X2 stimulations, there were no regional or sex differences in dopamine release. However, with CsChrimson, dopamine release was significantly higher in the corner than the medial tip, and females had more dopamine than males. Michaelis-Menten modeling of the single-light pulse revealed no significant regional differences in Km, but the corner had a significantly lower Vmax (0.12 μM/s vs. 0.19 μM/s) and higher dopamine release (0.05 μM vs. 0.03 μM). Optogenetic experiments are challenging because CsChrimson is also sensitive to blue light used to activate green fluorescent protein, and thus, light exposure during brain dissection must be minimized. These experiments expand the toolkit for measuring endogenous dopamine release in Drosophila, introducing chemogenetic and optogenetic experiments for the first time. With a variety of stimulations, different experiments will help improve our understanding of neurochemical signaling in Drosophila.

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Tyrosine hydroxylase immunostaining in the central complex of dicondylian insects

Timm

Scherner

Matschke

et al. 2021

J of Comparative Neurology

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Dopamine acts as a neurohormone and neurotransmitter in the insect nervous system and controls a variety of physiological processes. Dopaminergic neurons also innervate the central complex (CX), a multisensory center of the insect brain involved in sky compass navigation, goal‐directed locomotion and sleep control. To infer a possible influence of evolutionary history and lifestyle on the neurochemical architecture of the CX, we have studied the distribution of neurons immunoreactive to tyrosine hydroxylase (TH), the rate‐limiting enzyme in dopamine biosynthesis. Analysis of representatives from 12 insect orders ranging from firebrats to flies revealed high conservation of immunolabeled neurons. One type of TH‐immunoreactive neuron was found in all species studied. The neurons have somata in the pars intercerebralis, arborizations in the lateral accessory lobes, and axonal ramifications in the central body and noduli. In all pterygote species, a second type of tangential neuron of the upper division of the central body was TH‐immunoreactive. The neurons have cell bodies near the calyces and arborizations in the superior protocerebrum. Both types of neuron showed species‐specific variations in cell number and in the innervated areas outside and inside the CX. Additional neurons were found in only two taxa: one type of columnar neuron showed TH immunostaining in the water strider Gerris lacustris, but not in other Heteroptera, and a tritocerebral neuron innervating the protocerebral bridge was immunolabeled in Diptera. The data show largely taxon‐specific variations of a common ground pattern of putatively dopaminergic neurons that may be commonly involved in state‐dependent modulation of CX function.

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Independent Contributions of Discrete Dopaminergic Circuits to Cellular Plasticity, Memory Strength, and Valence in Drosophila

Cited by 41 publications

References 45 publications

Valence and state-dependent population coding in dopaminergic neurons in the fly mushroom body

Valence and state-dependent population coding in dopaminergic neurons in the fly mushroom body

Real-Time Measurement of Stimulated Dopamine Release in Compartments of the AdultDrosophila melanogasterMushroom Body

Tyrosine hydroxylase immunostaining in the central complex of dicondylian insects

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