Localization of Motor Neurons and Central Pattern Generators for Motor Patterns Underlying Feeding Behavior in Drosophila Larvae

Hückesfeld, Sebastian; Schoofs, Andreas; Schlegel, Philipp; Miroschnikow, Anton; Pankratz, Michael J.

doi:10.1371/journal.pone.0135011

“…All hugin neurons receive inputs within the subesophageal zone [SEZ, previously called subesophageal ganglion (SOG)], a chemosensory center that also houses the basic neuronal circuits generating feeding behavior [39]. However, only the hugin-PC neurons showed considerable numbers of synaptic outputs in the SEZ, consistent with their previously reported effects on feeding [19,40] (Fig.…”

Section: Resultssupporting

confidence: 79%

Synaptic Transmission Parallels Neuromodulation in a Central Food-Intake Circuit

Schlegel

¹

,

Texada

²

,

Miroschnikow

³

et al. 2016

Preprint

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NeuromedinU is a potent regulator of food intake and activity in mammals. In Drosophila, neurons producing the homologous neuropeptide hugin regulate feeding and locomotion in a similar manner. Here, we use EM-based reconstruction to generate the entire connectome of hugin-producing neurons in the Drosophila larval CNS. We demonstrate that hugin neurons use synaptic transmission in addition to peptidergic neuromodulation and identify acetylcholine as a key transmitter. Hugin neuropeptide and acetylcholine are both necessary for the regulatory effect on feeding. We further show that subtypes of hugin neurons connect chemosensory to endocrine system by combinations of synaptic and peptide-receptor connections. Targets include endocrine neurons producing DH44, a CRH-like peptide, and insulin-like peptides. Homologs of these peptides are likewise downstream of neuromedinU, revealing striking parallels in flies and mammals. We propose that hugin neurons are part of an ancient physiological control system that has been conserved at functional and molecular level.

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“…All hugin neurons receive inputs within the SEZ [previously called subesophageal ganglion (SOG)], a chemosensory center that also houses the basic neuronal circuits generating feeding behavior (Hückesfeld et al, 2015). However, only the hugin-PC neurons showed considerable numbers of synaptic outputs in the SEZ, consistent with their previously reported effects on feeding (Schoofs et al, 2014; Hückesfeld et al, 2016) (Figure 2E).…”

Section: Resultsmentioning

confidence: 99%

Synaptic transmission parallels neuromodulation in a central food-intake circuit

Schlegel

¹

,

Texada

²

,

Miroschnikow

³

et al. 2016

eLife

Self Cite

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NeuromedinU is a potent regulator of food intake and activity in mammals. In Drosophila, neurons producing the homologous neuropeptide hugin regulate feeding and locomotion in a similar manner. Here, we use EM-based reconstruction to generate the entire connectome of hugin-producing neurons in the Drosophila larval CNS. We demonstrate that hugin neurons use synaptic transmission in addition to peptidergic neuromodulation and identify acetylcholine as a key transmitter. Hugin neuropeptide and acetylcholine are both necessary for the regulatory effect on feeding. We further show that subtypes of hugin neurons connect chemosensory to endocrine system by combinations of synaptic and peptide-receptor connections. Targets include endocrine neurons producing DH44, a CRH-like peptide, and insulin-like peptides. Homologs of these peptides are likewise downstream of neuromedinU, revealing striking parallels in flies and mammals. We propose that hugin neurons are part of an ancient physiological control system that has been conserved at functional and molecular level.DOI: http://dx.doi.org/10.7554/eLife.16799.001

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“…However, any type or layer of neuron could theoretically participate in a CPG. Feeding in Drosophila larvae has been shown to make use of a CPG in the SEZ (Schoofs et al 2010(Schoofs et al , H€ uckesfeld et al 2015. In the SEZ of an adult moth, an interneuron was recorded that showed phasic activity to a tonic sugar stimulus (Kvello et al 2010), making it a good candidate for a component of a CPG.…”

Section: Interneuronsmentioning

confidence: 99%

Motor control of fly feeding

McKellar¹

2016

Journal of Neurogenetics

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Following considerable progress on the molecular and cellular basis of taste perception in fly sensory neurons, the time is now ripe to explore how taste information, integrated with hunger and satiety, undergo a sensorimotor transformation to lead to the motor actions of feeding behavior. I examine what is known of feeding circuitry in adult flies from more than 250 years of work in larger flies and from newer work in Drosophila. I review the anatomy of the proboscis, its muscles and their functions (where known), its motor neurons, interneurons known to receive taste inputs, interneurons that diverge from taste circuitry to provide information to other circuits, interneurons from other circuits that converge on feeding circuits, proprioceptors that influence the motor control of feeding, and sites of integration of hunger and satiety on feeding circuits. In spite of the several neuron types now known, a connected pathway from taste inputs to feeding motor outputs has yet to be found. We are on the threshold of an era where these individual components will be assembled into circuits, revealing how nervous system architecture leads to the control of behavior.

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Localization of Motor Neurons and Central Pattern Generators for Motor Patterns Underlying Feeding Behavior in Drosophila Larvae

Cited by 36 publications

References 39 publications

Synaptic Transmission Parallels Neuromodulation in a Central Food-Intake Circuit

Synaptic Transmission Parallels Neuromodulation in a Central Food-Intake Circuit

Synaptic transmission parallels neuromodulation in a central food-intake circuit

Motor control of fly feeding

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