Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit

Hiramoto, Atsuki; Jonaitis, Julius; Niki, Sawako; Kohsaka, Hiroshi; Fetter, Richard D.; Cardona, Albert; Pulver, Stefan R.; Nose, Akinao

doi:10.1038/s41467-021-23273-y

Cited by 20 publications

(14 citation statements)

References 56 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…A31k was identified as a GABAergic IN connected to aCC (Schneider-Mizell et al, 2016) and later shown to inhibit motor activity (Clark et al, 2018, Zarin et al, 2019 downstream of 'canon' neurons (Hiramoto et al, 2021). We tested three different drivers to verify A31k to aCC connectivity: R87H09-Gal4 (Zarin et al, 2019); R20A03-AD; R87H09-DBD split Gal4 (unpublished) and R20A03-AD; R93B07-DBD split Gal4 (a.k.a.…”

Section: A31k Is Monosynaptically Connected To Accmentioning

confidence: 99%

Electrophysiological Validation of Monosynaptic Connectivity between Premotor Interneurons and the aCC Motoneuron in the Drosophila Larval CNS

et al. 2022

Self Cite

View full text Add to dashboard Cite

The Drosophila connectome project aims to map the synaptic connectivity of entire larval and adult fly neural networks, which is essential for understanding nervous system development and function.So far, the project has produced an impressive amount of electron microscopy data that has facilitated reconstructions of specific synapses, including many in the larval locomotor circuit. While this breakthrough represents a technical tour-de-force, the data remain under-utilised, partly due to a lack of functional validation of reconstructions. Attempts to validate connectivity posited by the connectome project, have mostly relied on behavioural assays and/or GRASP or GCaMP imaging.While these techniques are useful, they have limited spatial or temporal resolution.Electrophysiological assays of synaptic connectivity overcome these limitations. Here, we combine patch clamp recordings with optogenetic stimulation in male and female larvae, to test synaptic connectivity proposed by connectome reconstructions. Specifically, we use multiple driver lines to confirm that several connections between premotor interneurons and the anterior corner cell (aCC) motoneuron are, as the connectome project suggests, monosynaptic. In contrast, our results also show that conclusions based on GRASP imaging may provide false positive results regarding connectivity between cells. We also present a novel imaging tool, based on the same technology as our electrophysiology, as a favourable alternative to GRASP. Finally, of eight Gal4 lines tested, five are reliably expressed in the premotors they are targeted to. Thus, our work highlights the need to confirm functional synaptic connectivity, driver line specificity, and use of appropriate genetic tools to support connectome projects. JN-RM-2463-21 R1 4 2 Significance StatementThe Drosophila connectome project aims to provide a complete description of connectivity between neurons in an organism that presents experimental advantages over other models. It has reconstructed over 80 percent of the fly larva's synaptic connections by manual identification of anatomical landmarks present in serial section transmission electron microscopy (ssTEM) volumes of the larval CNS. We use a highly reliable electrophysiological approach to verify these connections, so provide useful insight into the accuracy of work based on ssTEM. We also present a novel imaging tool for validating excitatory monosynaptic connections between cells, and show that several genetic driver lines designed to target neurons of the larval connectome exhibit non-specific and/or unreliable expression.

show abstract

Section: A31k Is Monosynaptically Connected To Accmentioning

confidence: 99%

Electrophysiological Validation of Monosynaptic Connectivity between Premotor Interneurons and the aCC Motoneuron in the Drosophila Larval CNS

et al. 2022

Self Cite

View full text Add to dashboard Cite

show abstract

“…The model in this study could describe forward crawling, the most frequent behaviour in larvae. Recent neuroscience studies have revealed numerous neural circuit modules involved in distinct aspects of behaviour, including speed control [ 32 ], bilateral coordination [ 35 ], intrasegmental coordination [ 36 ], intersegmental coordination [ 31 ], backward crawling [ 58 , 59 ], turning [ 60 ], escaping [ 61 ], and sensory input-guided navigation [ 34 , 62 ]. By integrating these circuit modules, it would be possible to establish a neuromechanical model that reproduces multiple and natural larval behaviours.…”

Section: Discussionmentioning

confidence: 99%

A neuromechanical model for Drosophila larval crawling based on physical measurements

Sun

Liu

et al. 2022

BMC Biol

Self Cite

View full text Add to dashboard Cite

Background Animal locomotion requires dynamic interactions between neural circuits, the body (typically muscles), and surrounding environments. While the neural circuitry of movement has been intensively studied, how these outputs are integrated with body mechanics (neuromechanics) is less clear, in part due to the lack of understanding of the biomechanical properties of animal bodies. Here, we propose an integrated neuromechanical model of movement based on physical measurements by taking Drosophila larvae as a model of soft-bodied animals. Results We first characterized the kinematics of forward crawling in Drosophila larvae at a segmental and whole-body level. We then characterized the biomechanical parameters of fly larvae, namely the contraction forces generated by neural activity, and passive elastic and viscosity of the larval body using a stress-relaxation test. We established a mathematical neuromechanical model based on the physical measurements described above, obtaining seven kinematic values characterizing crawling locomotion. By optimizing the parameters in the neural circuit, our neuromechanical model succeeded in quantitatively reproducing the kinematics of larval locomotion that were obtained experimentally. This model could reproduce the observation of optogenetic studies reported previously. The model predicted that peristaltic locomotion could be exhibited in a low-friction condition. Analysis of floating larvae provided results consistent with this prediction. Furthermore, the model predicted a significant contribution of intersegmental connections in the central nervous system, which contrasts with a previous study. This hypothesis allowed us to make a testable prediction for the variability in intersegmental connection in sister species of the genus Drosophila. Conclusions We generated a neurochemical model based on physical measurement to provide a new foundation to study locomotion in soft-bodied animals and soft robot engineering.

show abstract

“…The model in this study could describe forward crawling, the most frequent behaviour in larvae. Recent neuroscience studies have revealed numerous neural circuit modules involved in distinct aspects of behaviour, including speed control (32), bilateral coordination (35), intrasegmental coordination (36), intersegmental coordination (31), backward crawling (58, 59), turning (60), escaping (61), and sensory input guided navigation (34, 62). By integrating these circuit modules, we would be able to establish a neuromechanical model that reproduces multiple and natural larval behaviour.…”

Section: Discussionmentioning

confidence: 99%

A neuromechanical model forDrosophilalarval crawling based on physical measurements

Sun

Liu

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Animal locomotion requires dynamic interactions between neural circuits, muscles, and surrounding environments. In contrast to intensive studies on neural circuits, the neuromechanical basis for animal behaviour remains unclear due to the lack of information on the physical properties of animals. Here, taking Drosophila larvae as a model system, we proposed an integrated neuromechanical model based on physical measurements. The physical parameters were obtained by a stress-relaxation assay, and the neural circuit motif was extracted from a chain of excitatory and inhibitory interneurons, which was identified previously by connectomics. Based on the model, we systematically performed perturbation analyses on the parameters in the model to study their kinematic effects on locomotion performance. We found that modification of most of the parameters in the simulation could increase the speed of locomotion. Our physical measurement and modelling would provide a new framework for neural circuit studies and soft robot engineering.

show abstract

Regulation of coordinated muscular relaxation in Drosophila larvae by a pattern-regulating intersegmental circuit

Cited by 20 publications

References 56 publications

Electrophysiological Validation of Monosynaptic Connectivity between Premotor Interneurons and the aCC Motoneuron in the Drosophila Larval CNS

Electrophysiological Validation of Monosynaptic Connectivity between Premotor Interneurons and the aCC Motoneuron in the Drosophila Larval CNS

A neuromechanical model for Drosophila larval crawling based on physical measurements

A neuromechanical model forDrosophilalarval crawling based on physical measurements

Contact Info

Product

Resources

About