The Feeding Connectome: Convergence of Monosynaptic and Polysynaptic Sensory Paths onto Common Motor Outputs

Miroschnikow, Anton; Schlegel, Philipp; Schoofs, Andreas; Hückesfeld, Sebastian; F, Li; Schneider-Mizell, Casey M; Fetter, Richard D.; Truman, James W.; Cardona, Albert; Mj, Pankratz

doi:10.1101/368878

Cited by 4 publications

(7 citation statements)

References 64 publications

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“…Third, the hypothalamus-pituitary axis represents the main neuroendocrine system for metabolic homeostasis. Similar broad organization can be found in the Drosophila larva: the pharyngeal nerves of the SEZ also house both motor and sensory neurons that innervate external feeding organs and internal foregut structures [41,44,46,48,99,100]; a branch of the pharyngeal nerve also extends down to the ll R836 Current Biology 30, R831-R840, July 20, 2020 Review midgut in a manner similar to the vagus nerve [51]; and there is a central neuroendocrine axis that connects the brain to the major endocrine organ (the ring gland) [33,101]. As can be seen for both mammals and arthropods, the structures responsible for ancient functions like nutrient intake and homeostasis are located at the most basal, or inner, part of the brain and border the area for locomotion (the spinal cord and the ventral nerve cord) [102] (Figure 5C).…”

Section: Connectome Of a Neuropeptidergic Feeding Networkmentioning

confidence: 64%

“…Second, the extensive nature of the sensory inputs onto the hugin-PC neuronal network was revealed. Initial functional and anatomical data showed that hugin-PC neurons receive inputs from gustatory receptor neurons localized in the external and pharyngeal sense organs; however, the connectome data show that the greatest input is from the ENS [46,70]. Furthermore, whereas external and pharyngeal gustatory organs input onto the hugin-PC neurons and their immediate downstream partners, the enteric sensory organs input onto the entire hugin-PC neuronal network (Figure 4C).…”

Section: Connectome Of a Neuropeptidergic Feeding Networkmentioning

confidence: 99%

“…For example, the antennal nerve (AN) carries sensory projections from the olfactory organs (dorsal organs) as well as from the enteric nervous system [43][44][45]. These sensory inputs to the CNS can be subdivided into three categories based on their origin: external, pharyngeal and enteric (Figure 1C) [46][47][48].…”

Section: Larval Feeding Behavior and Organization Of The Feeding Motor Systemmentioning

confidence: 99%

“…In Drosophila, comprehensive synaptic mapping of the central feeding circuits became possible with the availability of a serial section transmission electron microscopic volume of a whole larval CNS [19]. Critically, the entry points of the pharyngeal nerves were intact in this volume, making it possible to trace and reconstruct all neurons projecting from the periphery to the CNS (i.e., sensory neurons) and vice versa (i.e., motor-/modulatory neurons) [43,46,56]. A subset of neurons targeting the ring gland were also reconstructed [56].…”

Section: The Feeding Connectomementioning

confidence: 99%

“…We can use one of the neurosecretory cells producing Dilps to illustrate the architecture of the core feeding network in more concrete terms. A Dilp cell receives direct inputs from a set of enteric sensory neurons [46,56]. At the same time, that Dilp cell receives indirect inputs from a set of pharyngeal sensory neurons via interneurons.…”

Section: The Feeding Connectomementioning

confidence: 99%

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Making Feeding Decisions in the Drosophila Nervous System

2020

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Feeding is one of the most fundamental activities of animals. Whether an animal will eat or not depends on sensory cues concerning nutrient availability and quality as well as on its growth, hormonal and metabolic state. These diverse signals, which originate from different regions of the body and act on different time scales, must be integrated by the nervous system to enable an appropriate feeding response. Here, we review recent studies in Drosophila melanogaster larvae that aim to elucidate the central circuits that underlie food intake, based on a serial section electron microscopic volume of an entire central nervous system. We focus on the comprehensive mapping of the synaptic connections between the sensory inputs and motor outputs of the larval feeding system. The central feeding circuit can be organized into a series of parallel pathways that connect a given set of input and output neurons. A dominant circuit motif is that of a monosynaptic sensory-motor connection upon which a series of polysynaptic paths are superimposed. The interneurons of the different parallel paths receive slightly different sets of sensory inputs, which enable flexibility in the selection of feeding motor outputs.

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Section: Connectome Of a Neuropeptidergic Feeding Networkmentioning

confidence: 64%

Section: Connectome Of a Neuropeptidergic Feeding Networkmentioning

confidence: 99%

Section: Larval Feeding Behavior and Organization Of The Feeding Motor Systemmentioning

confidence: 99%

Section: The Feeding Connectomementioning

confidence: 99%

Section: The Feeding Connectomementioning

confidence: 99%

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Making Feeding Decisions in the Drosophila Nervous System

2020

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Neural substrates of cold nociception inDrosophilalarva

Patel

Cardona

Cox

2023

Preprint

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Metazoans detect and differentiate between innocuous (non-painful) and/or noxious (harmful) environmental cues using primary sensory neurons, which serve as the first node in a neural network that computes stimulus specific behaviors to either navigate away from injury-causing conditions or to perform protective behaviors that mitigate extensive injury. The ability of an animal to detect and respond to various sensory stimuli depends upon molecular diversity in the primary sensors and the underlying neural circuitry responsible for the relevant behavioral action selection. Recent studies inDrosophilalarvae have revealed that somatosensory class III multidendritic (CIII md) neurons function as multimodal sensors regulating distinct behavioral responses to innocuous mechanical and nociceptive thermal stimuli. Recent advances in circuit bases of behavior have identified and functionally validatedDrosophilalarval somatosensory circuitry involved in innocuous (mechanical) and noxious (heat and mechanical) cues. However, central processing of cold nociceptive cues remained unexplored. We implicate multisensory integrators (Basins), premotor (Down-and-Back) and projection (A09e and TePns) neurons as neural substrates required for cold-evoked behavioral and calcium responses. Neural silencing of cell types downstream of CIII md neurons led to significant reductions in cold-evoked behaviors and neural co-activation of CIII md neurons plus additional cell types facilitated larval contraction (CT) responses. We further demonstrate that optogenetic activation of CIII md neurons evokes calcium increases in these neurons. Collectively, we demonstrate howDrosophilalarvae process cold stimuli through functionally diverse somatosensory circuitry responsible for generating stimulus specific behaviors.

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Neural substrates of cold nociception in Drosophila larva

Patel,

Cardona,

Cox

2023

Preprint

Self Cite

View full text Add to dashboard Cite

Metazoans detect and differentiate between innocuous (non-painful) and/or noxious (harmful) environmental cues using primary sensory neurons, which serve as the first node in a neural network that computes stimulus specific behaviors to either navigate away from injury-causing conditions or to perform protective behaviors that mitigate extensive injury. The ability of an animal to detect and respond to various sensory stimuli depends upon molecular diversity in the primary sensors and the underlying neural circuitry responsible for the relevant behavioral action selection. Recent studies in Drosophila larvae have revealed that somatosensory class III multidendritic (CIII md) neurons function as multimodal sensors regulating distinct behavioral responses to innocuous mechanical and nociceptive thermal stimuli. Recent advances in circuit bases of behavior have identified and functionally validated Drosophila larval somatosensory circuitry involved in innocuous (mechanical) and noxious (heat and mechanical) cues. However, central processing of cold nociceptive cues remained unexplored. We implicate multisensory integrators (Basins), premotor (Down-and-Back) and projection (A09e and TePns) neurons as neural substrates required for cold-evoked behavioral and calcium responses. Neural silencing of cell types downstream of CIII md neurons led to significant reductions in cold-evoked behaviors and neural co-activation of CIII md neurons plus additional cell types facilitated larval contraction (CT) responses. We further demonstrate that optogenetic activation of CIII md neurons evokes calcium increases in these neurons. Collectively, we demonstrate how Drosophila larvae process cold stimuli through functionally diverse somatosensory circuitry responsible for generating stimulus specific behaviors.

show abstract

The Feeding Connectome: Convergence of Monosynaptic and Polysynaptic Sensory Paths onto Common Motor Outputs

Cited by 4 publications

References 64 publications

Making Feeding Decisions in the Drosophila Nervous System

Making Feeding Decisions in the Drosophila Nervous System

Neural substrates of cold nociception inDrosophilalarva

Neural substrates of cold nociception in Drosophila larva

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