Anatomical and genotype-specific mechanosensory responses in Drosophila melanogaster larvae

Titlow, Josh; Rice, Jordan; Majeed, Zana R.; Holsopple, Emily; Biecker, Stephanie; Cooper, Robin L.

doi:10.1016/j.neures.2014.04.003

Cited by 20 publications

(20 citation statements)

References 30 publications

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“…Similarly to worms and lampreys, fly larvae respond to touch in different body parts with specific escape behaviors. Namely, both gentle (Kernan et al, 1994;Ma et al, 2016) and noxious (Titlow et al, 2014) head touch elicit backward locomotion, whereas tail touch elicits forward locomotion (Titlow et al, 2014). We found a segmentally repeated neuron, that we named Wave, whose activation in anterior segments sufficed to elicit backward locomotion, and in posterior segments sufficed to elicit forward locomotion.…”

Section: Introductionmentioning

confidence: 81%

“…On soft substrates, the wandering larvae mainly perform forward locomotion (Berni et al, 2012), whereas backward locomotion is infrequent except when encountering noxious and/or mechanical stimuli (Green et al, 1983;Kernan et al, 1994;Ma et al, 2016). A noxious touch (such as a pinprick) or a gentle touch to a behaving larva yields distinct responses depending on the location of the stimulation on the body (Titlow et al, 2014). The larvae transiently perform backward locomotion in response to touch on the larval head (which is defined here as the anterior end of the larva), whereas they escape by forward locomotion to touch on the tail ( Figure 1A).…”

Section: Different Larval Responses Are Induced By Noxious Touch Depementioning

confidence: 99%

“…A behavioral response to a given sensory cue often consists of multiple motor programs. In the case of Drosophila larvae, a mechanical noxious touch (such as a pinprick) not only induces backward or forward locomotion, but also rolling (Hwang et al, 2007;Kim et al, 2012;Ohyama et al, 2015;Robertson et al, 2013;Titlow et al, 2014;Tracey et al, 2003), depending on the strength and location of the stimuli. Hence, the basis of selection between locomotion or rolling escape behaviors should be implemented by the circuit architecture, possibly via lateral interaction between command neurons.…”

Section: Lateral Interaction Between Distinct Command Systemsmentioning

confidence: 99%

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Divergent Connectivity of Homologous Command-like Neurons Mediates Segment-Specific Touch Responses in Drosophila

Takagi

Cocanougher

Niki

et al. 2017

Neuron

116

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Animals adaptively respond to a tactile stimulus by choosing an ethologically relevant behavior depending on the location of the stimuli. Here, we investigate how somatosensory inputs on different body segments are linked to distinct motor outputs in Drosophila larvae. Larvae escape by backward locomotion when touched on the head, while they crawl forward when touched on the tail. We identify a class of segmentally repeated second-order somatosensory interneurons, that we named Wave, whose activation in anterior and posterior segments elicit backward and forward locomotion, respectively. Anterior and posterior Wave neurons extend their dendrites in opposite directions to receive somatosensory inputs from the head and tail, respectively. Downstream of anterior Wave neurons, we identify premotor circuits including the neuron A03a5, which together with Wave, is necessary for the backward locomotion touch response. Thus, Wave neurons match their receptive field to appropriate motor programs by participating in different circuits in different segments.

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Section: Introductionmentioning

confidence: 81%

Section: Different Larval Responses Are Induced By Noxious Touch Depementioning

confidence: 99%

Section: Lateral Interaction Between Distinct Command Systemsmentioning

confidence: 99%

See 1 more Smart Citation

Divergent Connectivity of Homologous Command-like Neurons Mediates Segment-Specific Touch Responses in Drosophila

Takagi

Cocanougher

Niki

et al. 2017

Neuron

116

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“…We also used direct electrical motor neuron stimulation using a suction electrode. Physiologically NMJs are stimulated in bouts at <42 Hz (Titlow et al, 2014).…”

Section: Metabolic and Neuronal Stimulation Induce The Formation Of Amentioning

confidence: 99%

“…We also used direct electrical motor neuron stimulation using a suction electrode. Physiologically NMJs are stimulated in bouts at <42 Hz (Titlow et al, 2014).Therefore, we challenged synapses by using a continuous 20 min 20 Hz stimulation paradigm.Again, these conditions induce macroautophagy at synaptic boutons ( Figure 1K-K''). Given that in these experiments the motor nerves are severed, our data indicate that our stimulation and starvation conditions reveal the local production of autophagosomes at synapses.…”

mentioning

confidence: 99%

A LRRK2-Dependent EndophilinA Phosphoswitch Is Critical for Macroautophagy at Presynaptic Terminals

Soukup

Kuenen

Vanhauwaert

et al. 2016

Neuron

218

285

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Manuscript 2Synapses are often far from the soma and independently cope with proteopathic stress induced by intense neuronal activity. However, how presynaptic compartments turnover proteins is poorly understood. We show that the synapse-enriched protein EndophilinA, thus far studied for its role in endocytosis, induces macroautophagy at presynaptic terminals. We find that EndophilinA executes this unexpected function at least partly independent of its role in synaptic vesicle endocytosis. EndophilinA-induced macroautophagy is activated when the kinase LRRK2 phosphorylates the EndophilinA-BAR domain and is blocked in animals where EndophilinA cannot be phosphorylated. EndophilinA INTRODUCTIONNeurons can be metabolically very active, firing at rates of more than 100 Hz.Synaptic proteins and organelles are used and re-used multiple times and accumulate damage as a result of this stress. Furthermore, synapses are often located far away from the cell body and must therefore in part operate independently. This raises the question how synapses maintain protein quality. Given that neurodegeneration is thought to start with subtle synaptic defects before evolving into blunt neuronal death (Burke and O'Malley, 2013;, the mechanisms of synaptic protein homeostasis are likely relevant for the understanding of neurodegenerative disease.Macroautophagy is well-placed to mediate protein turnover, but how the needs of synapses are served by this process has not been well-studied. Cellular signals like stress and amino acid deprivation induce macroautophagy, where cytoplasm is engulfed by double membrane structures before fusion with degradative lysosomes (Mizushima et al., 2011).Autophagosomes have been visualized using fluorescent markers in yeast, Drosophila and mammalian cells and are often observed as Atg8/LC3 positive puncta (Kabeya et al., 2000;Scott et al., 2004). At the stage of initiation, Atg9-positive vesicles fuse into elongated preautophagosomal structures with growing edges (He et al., 2006). These edges are highly curved and harbor lipid packing defects. These edges serve as protein docking sites, attracting specific autophagic factors such as Atg3, Atg14/Barkor and Atg1 that insert into such zones, recognizing specific lipids (phosphatidylinositol-3-phosphate (PI(3)P)) and lipid packing defects (Fan et al., 2011;Nath et al., 2014;Ragusa et al., 2012). The recruitment of these factors then promotes the further steps of autophagosome formation; in particular the E2-like protein Atg3 itself recruits the autophagic marker LC3/Atg8 (Nath et al., 2014). However, how these highly curved edges are formed and maintained is very poorly understood.While autophagy has been mostly analyzed in the soma of cultured cells and yeast, autophagic markers have also been observed away from the soma at neuronal synapses 4 (Hernandez et al., 2012;Maday and Holzbaur, 2014;Williamson et al., 2010) and these markers were shown to be transported along axons (Maday and Holzbaur, 2014). However, how autophagosomes are formed at synapses an...

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Using optogenetics to assess neuroendocrine modulation of heart rate in Drosophila melanogaster larvae

et al. 2017

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The Drosophila melanogaster heart has become a principal model in which to study cardiac physiology and development. While the morphology of the heart in Drosophila and mammals is different, many of the molecular mechanisms that underlie heart development and function are similar and function can be assessed by similar physiological measurements, such as cardiac output, rate, and time in systole or diastole. Here, we have utilized an intact, optogenetic approach to assess the neural influence on heart rate in the third instar larvae. To simulate the release of modulators from the nervous system in response to environmental influences, we have directed expression of channel-rhodopsin variants to targeted neuronal populations to assess the role of these neural ensembles in directing release of modulators that may affect heart rate in vivo. Our observations show that the activation of targeted neurons, including cholinergic, dopaminergic, and serotonergic neurons, stimulate the release of cardioactive substances that increase heart rate after the initial activation at both room temperature and in a cold environment. This parallels previous studies suggesting these modulators play a crucial role in altering heart rate when applied to exposed hearts and adds to our understanding of chemical modulation of heart rate in intact Drosophila larvae.

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Anatomical and genotype-specific mechanosensory responses in Drosophila melanogaster larvae

Cited by 20 publications

References 30 publications

Divergent Connectivity of Homologous Command-like Neurons Mediates Segment-Specific Touch Responses in Drosophila

Divergent Connectivity of Homologous Command-like Neurons Mediates Segment-Specific Touch Responses in Drosophila

A LRRK2-Dependent EndophilinA Phosphoswitch Is Critical for Macroautophagy at Presynaptic Terminals

Using optogenetics to assess neuroendocrine modulation of heart rate in Drosophila melanogaster larvae

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