The development of motor coordination in <i>Drosophila</i>embryos

Crisp, Sarah; Evers, Jan Felix; Fiala, André; Bate, Michael

doi:10.1242/dev.026773

Cited by 97 publications

(143 citation statements)

References 46 publications

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“…1 D). Onset of Eaat1 transcript expression occurred rather late in embryogenesis (stages 15-16), which is consistent with previous reports (Besson et al, 1999;Soustelle et al, 2002), and only narrowly precedes the initiation of spontaneous and uncoordinated muscle contractions (Crisp et al, 2008).…”

Section: Eaat1 Expression In Drosophila Cnssupporting

confidence: 92%

DrosophilaGlial Glutamate Transporter Eaat1 Is Regulated by Fringe-Mediated Notch Signaling and Is Essential for Larval Locomotion

Stacey¹,

Muraro²,

Peco³

et al. 2010

J. Neurosci.

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In the mammalian CNS, glial cells expressing excitatory amino acid transporters (EAATs) tightly regulate extracellular glutamate levels to control neurotransmission and protect neurons from excitotoxic damage. Dysregulated EAAT expression is associated with several CNS pathologies in humans, yet mechanisms of EAAT regulation and the importance of glutamate transport for CNS development and function in vivo remain incompletely understood. Drosophila is an advanced genetic model with only a single high-affinity glutamate transporter termed Eaat1. We found that Eaat1 expression in CNS glia is regulated by the glycosyltransferase Fringe, which promotes neuron-to-glia signaling through the Delta-Notch ligand-receptor pair during embryogenesis. We made Eaat1 loss-of-function mutations and found that homozygous larvae could not perform the rhythmic peristaltic contractions required for crawling. We found no evidence for excitotoxic cell death or overt defects in the development of neurons and glia, and the crawling defect could be induced by postembryonic inactivation of Eaat1. Eaat1 fully rescued locomotor activity when expressed in only a limited subpopulation of glial cells situated near potential glutamatergic synapses within the CNS neuropil. Eaat1 mutants had deficits in the frequency, amplitude, and kinetics of synaptic currents in motor neurons whose rhythmic patterns of activity may be regulated by glutamatergic neurotransmission among premotor interneurons; similar results were seen with pharmacological manipulations of glutamate transport. Our findings indicate that Eaat1 expression is promoted by Fringe-mediated neuron-glial communication during development and suggest that Eaat1 plays an essential role in regulating CNS neural circuits that control locomotion in Drosophila.

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Section: Eaat1 Expression In Drosophila Cnssupporting

confidence: 92%

DrosophilaGlial Glutamate Transporter Eaat1 Is Regulated by Fringe-Mediated Notch Signaling and Is Essential for Larval Locomotion

Stacey¹,

Muraro²,

Peco³

et al. 2010

J. Neurosci.

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“…Our model thus sharpens biological questions about the relative importance of centralized control and local/distributed sensory feedback for the development and maintenance of coordinated locomotion [19,20]. It also suggests alternative design of bioinspired robotic systems by replacing global coordination and actuation by decentralized modules where most of the control effort is replaced by elementary interactions of the body with the substrate that can trigger switch-like behaviour and thus lead to coordinated locomotion [24].…”

Section: Discussionmentioning

confidence: 72%

“…This robustness to the presence of diffusive neural connections might explain some experimental observations associated with the development of rhythmic patterns Although travelling waves of neural excitation are observed even in the absence of sensory stimulus [19,20], they are easily disrupted, and it is thought that sensory feedback is important to stabilize them. One possible scenario that accounts for this is that larvae start out with diffusive neural connections to trigger the rhythmic pattern during the early stages of development where sensory feedback is very limited or even absent.…”

Section: The Role Of Noise and Diffusive Neural Couplingmentioning

confidence: 94%

A proprioceptive neuromechanical theory of crawling

Paoletti

Mahadevan

2014

Proc. R. Soc. B.

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The locomotion of many soft-bodied animals is driven by the propagation of rhythmic waves of contraction and extension along the body. These waves are classically attributed to globally synchronized periodic patterns in the nervous system embodied in a central pattern generator (CPG). However, in many primitive organisms such as earthworms and insect larvae, the evidence for a CPG is weak, or even non-existent. We propose a neuromechanical model for rhythmically coordinated crawling that obviates the need for a CPG, by locally coupling the local neuro-muscular dynamics in the body to the mechanics of the body as it interacts frictionally with the substrate. We analyse our model using a combination of analytical and numerical methods to determine the parameter regimes where coordinated crawling is possible and compare our results with experimental data. Our theory naturally suggests mechanisms for how these movements might arise in developing organisms and how they are maintained in adults, and also suggests a robust design principle for engineered motility in soft systems.

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“…Based on the data shown here, we propose the following model: during the late stages of fly development, once the MTJs form, they are exposed to increasingly more powerful muscle contractions (Crisp et al, 2008). This applies more mechanical force on ligandbound integrins at the plasma membrane and results in conformational changes in the integrin that trigger an increase in outside-in signaling.…”

Section: Discussionmentioning

confidence: 96%

In vivo regulation of integrin turnover by outside-in activation

López-Ceballos¹,

Herrera-Reyes²,

Coombs³

et al. 2016

Development

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The development of three-dimensional tissue architecture requires precise control over the attachment of cells to the extracellular matrix (ECM). Integrins, the main ECM-binding receptors in animals, are regulated in multiple ways to modulate cell-ECM adhesion. One example is the conformational activation of integrins by extracellular signals ('outside-in activation') or by intracellular signals ('inside-out activation'), whereas another is the modulation of integrin turnover. We demonstrate that outside-in activation regulates integrin turnover to stabilize tissue architecture in vivo. Treating Drosophila embryos with Mg 2+ and Mn 2+, known to induce outside-in activation, resulted in decreased integrin turnover. Mathematical modeling combined with mutational analysis provides mechanistic insight into the stabilization of integrins at the membrane. We show that as tissues mature, outside-in activation is crucial for regulating the stabilization of integrin-mediated adhesions. This data identifies a new in vivo role for outside-in activation and sheds light on the key transition between tissue morphogenesis and maintenance.

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The development of motor coordination in Drosophilaembryos

Cited by 97 publications

References 46 publications

DrosophilaGlial Glutamate Transporter Eaat1 Is Regulated by Fringe-Mediated Notch Signaling and Is Essential for Larval Locomotion

DrosophilaGlial Glutamate Transporter Eaat1 Is Regulated by Fringe-Mediated Notch Signaling and Is Essential for Larval Locomotion

A proprioceptive neuromechanical theory of crawling

In vivo regulation of integrin turnover by outside-in activation

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