Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

Tsao, Chang-Hui; Chen, Chien-Chun; Lin, Chen-Han; Yang, Hao-Yu; Lin, Suewei

doi:10.7554/elife.35264

Cited by 160 publications

(216 citation statements)

References 130 publications

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“…Previous studies that focused on individual DANs implicated some of these compartments in metabolic state-dependent choice behavior (i.e. β'2) [13,18,46]. Our present results suggest that other compartments such as β'1 might also contribute in conveying feeding state to sensory processing.…”

supporting

confidence: 56%

“…20 Invertebrates including the fly Drosophila melanogaster use dopamine in highly analogous processes [1,6,9]. The exquisite tools of fly genetics have provided important insights into the role, molecular and circuit mechanisms of dopamine in associative learning and memory as well as state-dependent behavior (e.g., [10][11][12][13][14][15]). A focus of many studies has been a dense network of ~200 dopaminergic cells innervating the so-called mushroom body (MB) (Fig.…”

Section: Introductionmentioning

confidence: 99%

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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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supporting

confidence: 56%

Section: Introductionmentioning

confidence: 99%

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

Siju

Štih

Aimon

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Although the role of DANs in feeding behavior remains unclear, accumulating evidence suggests that MBONs can modulate innate behavior such as taste sensitivity (Masek et al, 2015), naïve response to odors (Owald et al, 2015), place preference (Aso et al, 2014b) or food seeking behavior (Tsao et al, 2018). Could the effect of DANs in the STROBE be mediated by a learning-driven process?…”

Section: Discussionmentioning

confidence: 99%

“…MBONs are required for memory formation and retrieval (Aso et al, 2014b;2014a;Bouzaiane et al, 2015;Felsenberg et al, 2017;Ichinose et al, 2015;Masek et al, 2015;Owald et al, 2015;Perisse et al, 2016;Plaçais et al, 2013;Séjourné et al, 2011;Takemura et al, 2017;Tanaka et al, 2008). In addition, MBONs can modulate innate behaviors such as taste sensitivity (Masek et al, 2015) or food seeking behavior (Tsao et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

The STROBE: a system for closed-looped optogenetic control of freely feeding flies

Musso

Junca

Jelen

et al. 2018

Preprint

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Manipulating feeding circuits in freely moving animals is challenging, in part because the timing of sensory inputs is affected by the animal's behavior. To address this challenge in Drosophila, we developed the Sip-Triggered Optogenetic Behavior Enclosure ("STROBE"). The STROBE is a closed-looped system for real-time optogenetic activation of feeding flies, designed to evoke neural excitation coincident with food contact. We demonstrate that optogenetic stimulation of sweet sensory neurons in the STROBE drives attraction to tasteless food, while activation of bitter sensory neurons promotes avoidance. Moreover, feeding behavior in the STROBE is modified by the fly's internal state, as well as the presence of chemical taste ligands. We also find that mushroom body dopaminergic neurons and their respective post-synaptic partners drive opposing feeding behaviors following activation. Together, these results establish the STROBE as a new tool for dissecting fly feeding circuits and suggest a role for mushroom body circuits in processing naïve taste responses.

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“…An arsenal of genetic tools to manipulate any gene's function within each of these cell subtypes already exists (109,110). In addition to olfactory associative memory, MBs also play fundamental roles in other forms of memory including visual and gustatory (9, 10), temperature preference (11), courtship behaviors (79,80), stress response (92), food-seeking (111), sleep (12) and responses to ethanol (13). This dataset will facilitate the discovery of neural mechanisms for each of these conserved behaviors.…”

Section: Several Previous Studies Have Used Genome-wide Methods To Prmentioning

confidence: 99%

Nuclear transcriptomes of the seven neuronal cell types that constitute theDrosophilamushroom bodies

Shih

Davis

Henry

et al. 2018

Preprint

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The insect mushroom body (MB) is a conserved brain structure that plays key roles in a diverse array of behaviors. The Drosophila melanogaster MB is the primary invertebrate model of neural circuits related to memory formation and storage, and its development, morphology, wiring, and function has been extensively studied. MBs consist of intrinsic Kenyon Cells that are divided into three major neuron classes (γ, α′/β′ and α/β) and 7 cell subtypes (γd, γm, α′/β′ap, α′/β′m, α/βp, α/βs and α/βc) based on their birth order, morphology, and connectivity. These subtypes play distinct roles in memory processing, however the underlying transcriptional differences are unknown. Here, we used RNA sequencing (RNA-seq) to profile the nuclear transcriptomes of each MB neuronal cell subtypes.We identified 350 MB class-or subtype-specific genes, including the widely used α/β class marker Fas2 and the α′/β′ class marker trio. Immunostaining corroborates the RNA-seq measurements at the protein level for several cases. Importantly, our data provide a full accounting of the neurotransmitter receptors, transporters, neurotransmitter biosynthetic enzymes, neuropeptides, and neuropeptide receptors expressed within each of these cell types. This high-quality, cell type-level transcriptome catalog for the Drosophila MB provides a valuable resource for the fly neuroscience community.

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Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

Cited by 160 publications

References 130 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

The STROBE: a system for closed-looped optogenetic control of freely feeding flies

Nuclear transcriptomes of the seven neuronal cell types that constitute theDrosophilamushroom bodies

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