Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons

Manjila, Steffy B.; Kuruvilla, Maria; Ferveur, Jean‐François; Sane, Sanjay P.; Hasan, Gaiti

doi:10.1016/j.cub.2018.11.070

Cited by 20 publications

(22 citation statements)

References 67 publications

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“…These studies identified the importance of modulated dopamine release as a motivational cue wherein dopamine release from PPL1- γ2α′1 DANs increased in starved flies ( Tsao et al, 2018 ) and inhibited the activity of a cholinergic output neuron from the Mushroom Body (MBON- γ2α′1; Tsao et al, 2018 ). The MBON- γ2α′1 projects to another set of central DANs, the PAM neurons ( Felsenberg et al, 2017 ), identified as flight promoting in a previous study ( Manjila et al, 2019 ), as well as the fan shaped body (FSB) and the lateral accessory lobe (LAL; Scaplen et al, 2020 ). This leads to the hypothesis that inputs regarding the internal state reach the PPL1- γ2α′1 DANs through mAChR, amongst other GPCR (see below), driven IP 3 /Ca 2+ signals to modulate dopamine release at the PPL1- γ2α′1 > MBON- γ2α′1 synapse, and the extent of dopamine release changes the output strength of MBON - γ2α′1.…”

Section: Discussionmentioning

confidence: 95%

Modulation of flight and feeding behaviours requires presynaptic IP3Rs in dopaminergic neurons

Sharma

Hasan

2020

eLife

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Innate behaviours, although robust and hard wired, rely on modulation of neuronal circuits, for eliciting an appropriate response according to internal states and external cues. Drosophila flight is one such innate behaviour that is modulated by intracellular calcium release through inositol 1,4,5-trisphosphate receptors (IP3Rs). Cellular mechanism(s) by which IP3Rs modulate neuronal function for specific behaviours remain speculative, in vertebrates and invertebrates. To address this, we generated an inducible dominant negative form of the IP3R (IP3RDN). Flies with neuronal expression of IP3RDN exhibit flight deficits. Expression of IP3RDN helped identify key flight-modulating dopaminergic neurons with axonal projections in the mushroom body. Flies with attenuated IP3Rs in these presynaptic dopaminergic neurons exhibit shortened flight bouts and a disinterest in seeking food, accompanied by reduced excitability and dopamine release upon cholinergic stimulation. Our findings suggest that the same neural circuit modulates the drive for food search and for undertaking longer flight bouts.

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Section: Discussionmentioning

confidence: 95%

Modulation of flight and feeding behaviours requires presynaptic IP3Rs in dopaminergic neurons

Sharma

Hasan

2020

eLife

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“…We have developed a method to trace active neural circuitry in freely-moving intact adult Drosophila . While previous methods have used direct laser light from microscopes, requiring immobilization of the fly (Bohra et al, 2018; Manjila et al, 2019), our method using LEDs and Petri dishes allows the flies to remain mobile and freely behaving and allows us to capture the active circuitry of multiple flies simultaneously. We demonstrate that this method faithfully recapitulates a previous study (Ai et al, 2010) demonstrating that exposure to acids activates the Ir64a-expressing neurons of the DC4 glomerulus in the antennal lobe of adult flies.…”

Section: Discussionmentioning

confidence: 99%

“…However use in adult fruit flies has been limited due to the head cuticle of the fly. Most published reports of CaMPARI’s uses in the adult fruit fly, require the fly to be fixed or tethered on a microscope with direct illumination from a laser (Bohra et al, 2018; Manjila et al, 2019). While such experiments are valuable, they limit the movement of the fly and again require the animal to be solitary, which can affect how an animal responds to stimulus naturally (Ramdya et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

The Photoconvertible Fluorescent Probe, CaMPARI, Labels Active Neurons in Freely-Moving Intact Adult Fruit Flies

Edwards

Hoppa

Bosco

2020

Preprint

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AbstractLinking neural circuitry to behavior by mapping active neurons in vivo is a challenge. Both genetically encoded calcium indicators (GECIs) and intermediate early genes (IEGs) have been used to pinpoint active neurons during a stimulus or a behavior but have drawbacks such as limiting the movement of the organism, requiring a priori knowledge of the active region or having poor temporal resolution. CaMPARI (calcium-modulated photoactivatable ratiometric integrator) was engineered to overcome these spatial-temporal challenges. CaMPARI is a photoconvertible protein that only converts from green to red fluorescence in the presence of high calcium concentration and violet (405 nm) light. This allows the experimenter to precisely mark active neurons within defined temporal windows. The photoconversion can then be quantified by taking the ratio of the red fluorescence to the green. CaMPARI promises the ability to trace active neurons during specific stimulus; however, CaMPARI’s uses in adult Drosophila have been limited to photoconversion during fly immobilization. Here, we demonstrate a method that allows photoconversion of multiple freely-moving intact adult flies during a stimulus. Flies were placed in a dish with filter paper wet with acetic acid (pH=2) or neutralized acetic acid (pH=7) and exposed to photoconvertible light (60 mW) for 30 min (500 ms on, 200 ms off). Immediately following photoconversion, whole flies were fixed and imaged by confocal microscopy. The red:green ratio was quantified for the DC4 glomerulus, a bundle of neurons expressing Ir64a, an ionotropic receptor that senses acids in the Drosophila antennal lobe. Flies exposed to acetic acid showed 1.3-fold greater photoconversion than flies exposed to neutralized acetic acid. This finding was recapitulated using a more physiological stimulus of apple cider vinegar. These results indicate that CaMPARI can be used to label neurons in intact, freely-moving adult flies and will be useful for identifying the circuitry underlying complex behaviors.

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“…The insect mushroom-bodies (MBs) are not only known as a center for olfactory learning and memory (Dolan et al, 2018;Felsenberg et al, 2018;König et al, 2019;Lyutova et al, 2019;Thum and Gerber, 2019;Turrel et al, 2018;e.g., Warth Pérez Arias et al, 2020;Widmer et al, 2018), they are also involved in the temporal and spatial control of locomotor activity (Besson and Martin, 2005;Helfrich-Förster et al, 2002;Lark et al, 2017;Lebreton and Martin, 2009;Mabuchi et al, 2016;Manjila et al, 2019;e.g., Martin et al, 1998;Serway et al, 2009;Sun et al, 2018;Xiong et al, 2010). In addition, (Castells-Nobau et al, 2019) (Fig.…”

Section: Foxp-ib Expression In the Drosophila Brainmentioning

confidence: 99%

“…The only case where only one set of parameters was affected were the FoxP 3955 mutant flies (Fig. 6) MBs have been shown to affect both spatial and temporal aspects of locomotion (Besson and Martin, 2005;Helfrich-Förster et al, 2002;Lark et al, 2017;Lebreton and Martin, 2009;Mabuchi et al, 2016;Manjila et al, 2019; e.g., Martin et al, 1998;Serway et al, 2009;Sun et al, 2018;Xiong et al, 2010) (Linneweber et al, 2020), but removing FoxP from DCNs showed no effect (Fig. 9B), despite abundant FoxP expression in DCNs (Fig.…”

Section: Foxp Expressionmentioning

confidence: 99%

Identification ofFoxPcircuits involved in locomotion and object fixation inDrosophila

Palazzo

Rass

Brembs

2020

Preprint

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The FoxP family of transcription factors is necessary for operant self-learning, an evolutionary conserved form of motor learning. The expression pattern, molecular function and mechanisms of action of the Drosophila FoxP orthologue remain to be elucidated. By editing the genomic locus of FoxP with CRISPR/Cas9, we find that the three different FoxP isoforms are expressed in neurons, but not in glia and that not all neurons express all isoforms. Furthermore, we detect FoxP expression in, e.g., the protocerebral bridge, the fan shaped body and in motorneurons, but not in the mushroom bodies. Finally, we discover that FoxP expression during development, but not adulthood, is required for normal locomotion and landmark fixation in walking flies. While FoxP expression in the protocerebral bridge and motorneurons is involved in locomotion and landmark fixation, the FoxP gene can be deleted from dorsal cluster neurons and mushroom-body Kenyon cells without affecting these behaviors.

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Extended Flight Bouts Require Disinhibition from GABAergic Mushroom Body Neurons

Cited by 20 publications

References 67 publications

Modulation of flight and feeding behaviours requires presynaptic IP3Rs in dopaminergic neurons

Modulation of flight and feeding behaviours requires presynaptic IP3Rs in dopaminergic neurons

The Photoconvertible Fluorescent Probe, CaMPARI, Labels Active Neurons in Freely-Moving Intact Adult Fruit Flies

Identification ofFoxPcircuits involved in locomotion and object fixation inDrosophila

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