A premotor microcircuit to generate behavior-specific muscle activation patterns in Drosophila larvae

Huang, Yuhan; Zarin, Aref Arzan

doi:10.1101/2022.08.18.504452

Cited by 4 publications

(4 citation statements)

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“…Of particular interest to researchers are the neural mechanisms and muscle kinematics underlying rolling behavior, which are currently being investigated in detail ( He et al, 2022 ; Cooney et al, 2023 ). How to generate multiple behavioral patterns using the same neural circuit is one of the fundamental questions in neuroscience ( Briggman and Kristan, 2008 ), and larval motor circuits can provide an excellent model system for studying this phenomenon ( Kohsaka et al, 2019 ; Zarin et al, 2019 ; Hiramoto et al, 2021 ; Huang and Zarin, 2022 ). While various larval behaviors exist, this review specifically focuses on larval locomotion, as its neural and physical mechanisms have been extensively examined.…”

Section: The Drosophila Larval Motor Systemsmentioning

confidence: 99%

Linking neural circuits to the mechanics of animal behavior in Drosophila larval locomotion

Kohsaka

2023

Front. Neural Circuits

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The motions that make up animal behavior arise from the interplay between neural circuits and the mechanical parts of the body. Therefore, in order to comprehend the operational mechanisms governing behavior, it is essential to examine not only the underlying neural network but also the mechanical characteristics of the animal’s body. The locomotor system of fly larvae serves as an ideal model for pursuing this integrative approach. By virtue of diverse investigation methods encompassing connectomics analysis and quantification of locomotion kinematics, research on larval locomotion has shed light on the underlying mechanisms of animal behavior. These studies have elucidated the roles of interneurons in coordinating muscle activities within and between segments, as well as the neural circuits responsible for exploration. This review aims to provide an overview of recent research on the neuromechanics of animal locomotion in fly larvae. We also briefly review interspecific diversity in fly larval locomotion and explore the latest advancements in soft robots inspired by larval locomotion. The integrative analysis of animal behavior using fly larvae could establish a practical framework for scrutinizing the behavior of other animal species.

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Section: The Drosophila Larval Motor Systemsmentioning

confidence: 99%

Linking neural circuits to the mechanics of animal behavior in Drosophila larval locomotion

Kohsaka

2023

Front. Neural Circuits

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“…Animal locomotive behavioral responses are implemented through neurosecretory systems and muscle contractions evoked by motor neuron activity. Motor neurons integrate a conglomerate of neural impulses from premotor neurons, leading to appropriate muscle activation patterns to implement specific behavioral responses (Bellardita & Kiehn, 2015;Berkowitz et al, 2010;Carreira-Rosario et al, 2018;Green & Soffe, 1996;Huang & Zarin, 2022;Liao & Fetcho, 2008;Talpalar et al, 2013;Zarin et al, 2019). Recent work in premotor and motor neuron connectomics has provided evidence for both labeled line and combinatorial connectivity between promotor and motor neurons that give rise to co-active motor neurons states leading to selective muscle group activation (Huang & Zarin, 2022;Zarin et al, 2019).…”

Section: Multisensory Integration Neurons Drive Behavioral Selection ...mentioning

confidence: 99%

“…Motor neurons integrate a conglomerate of neural impulses from premotor neurons, leading to appropriate muscle activation patterns to implement specific behavioral responses (Bellardita & Kiehn, 2015;Berkowitz et al, 2010;Carreira-Rosario et al, 2018;Green & Soffe, 1996;Huang & Zarin, 2022;Liao & Fetcho, 2008;Talpalar et al, 2013;Zarin et al, 2019). Recent work in premotor and motor neuron connectomics has provided evidence for both labeled line and combinatorial connectivity between promotor and motor neurons that give rise to co-active motor neurons states leading to selective muscle group activation (Huang & Zarin, 2022;Zarin et al, 2019). Various Drosophila larval premotor neuron subtypes and/or motor pools have been implicated in locomotion, nociception, and innocuous mechanosensation (Burgos et al, 2018;Huang & Zarin, 2022;Jovanic et al, 2019;Kohsaka et al, 2017;Kohsaka et al, 2014;Kohsaka et al, 2019;Yoshino et al, 2017;Zarin et al, 2019).…”

Section: Multisensory Integration Neurons Drive Behavioral Selection ...mentioning

confidence: 99%

“…Recent work in premotor and motor neuron connectomics has provided evidence for both labeled line and combinatorial connectivity between promotor and motor neurons that give rise to co-active motor neurons states leading to selective muscle group activation (Huang & Zarin, 2022;Zarin et al, 2019). Various Drosophila larval premotor neuron subtypes and/or motor pools have been implicated in locomotion, nociception, and innocuous mechanosensation (Burgos et al, 2018;Huang & Zarin, 2022;Jovanic et al, 2019;Kohsaka et al, 2017;Kohsaka et al, 2014;Kohsaka et al, 2019;Yoshino et al, 2017;Zarin et al, 2019). Neural reconstruction efforts in Drosophila larvae have revealed that somatosensory (CIII md and CIV md) neurons are not directly connected to motor neurons, but rather feed into polysynaptic pathways leading to motor neurons via premotor neurons (such as the DnB, mCSI, & Chair-1 neurons studied here) (Jovanic et al, 2019;Ohyama et al, 2015;Winding et al, 2022).…”

Section: Multisensory Integration Neurons Drive Behavioral Selection ...mentioning

confidence: 99%

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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

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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 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

A premotor microcircuit to generate behavior-specific muscle activation patterns in Drosophila larvae

Cited by 4 publications

References 58 publications

Linking neural circuits to the mechanics of animal behavior in Drosophila larval locomotion

Linking neural circuits to the mechanics of animal behavior in Drosophila larval locomotion

Neural substrates of cold nociception inDrosophilalarva

Neural substrates of cold nociception in Drosophila larva

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