Development of swimming behaviour in the larva of the ascidian<i>Ciona intestinalis</i>

Zega, Giuliana; Thorndyke, Michael C.; Brown, Euan R.

doi:10.1242/jeb.02421

Cited by 46 publications

(63 citation statements)

References 32 publications

(52 reference statements)

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“…When a long-pass filter was used to cut off the light visible to the larvae (<590 nm), they swam more vigorously in what is called a shading response (Movie S1) (11,15). In the "dark," the tail-beating frequency (ϕ) and the velocity of the traveling wave (ϖ) increased significantly (15), whereas the wavelength of the swimming cycles (λ = ϖ/ϕ) and the mean of the flexure strength (curvature) were relatively constant ( Fig. 1D and S2 A-C).…”

Section: Resultsmentioning

confidence: 99%

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

Nishino

Baba

Okamura

2011

Proc. Natl. Acad. Sci. U.S.A.

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The larva of the invertebrate chordate Ciona intestinalis possesses only 36 striated muscle cells and lacks body segmentation. It can swim, however, like a vertebrate tadpole, and how its simple body achieves such sophisticated motor control remains puzzling. We found that muscle contractions in Ciona larvae are variable and can be changed by sensory stimuli, so that neuromuscular transmission can convert the variable neural inputs into graded muscle activity. We characterized the molecular nature of the nicotinic acetylcholine receptor (nAChR) at neuromuscular synapses. When heterologously expressed in Xenopus oocytes, this nAChR channel exhibited two biophysical features resembling vertebrate neuronal nAChRs rather than the muscle type: inward rectification and high Ca 2+ permeability. Both of these properties were abolished by a simple mutation at the channel pore in one of the non-α subunits, called BGDE3, so as to adopt the sequence of related subunits in vertebrates, γ and ε. In vivo exchange of native BGDE3 with this mutant severely disrupted graded motor control, producing instead sporadic all-or-none-like flexions. The graded nature of excitation-contraction (E-C) coupling in this organism is based on the traits of the nAChR channel pore, which confer fine controllability on such a coarse motor architecture.ascidian larva | muscle physiology | locomotion | neuromuscular junction I n tailed aquatic vertebrates such as fish and amphibian tadpoles, swimming undulations are generated by sequential activation of the myotomal segments. These segments contain multiple classes of muscle fibers, including slow, fast, and intermediate types, with distinct mechanical and metabolic properties that constitute a "gearing" system adjustable to a wide range of speeds. The activity of a given segment is mostly independent of the others, and when, which, and how many fibers will be activated are determined by a neural network in the spinal cord (1-3). This neural mechanism by which contraction magnitude is varied is based on the logic for recruiting motor neurons into the active population, called the size principle (1-4). This control system for compound muscle fibers is likely a key innovation in vertebrates, but how far this basis can be traced back in invertebrate systems is poorly understood.Ascidians are marine invertebrates that constitute a sister clade of the vertebrates (5, 6). The larva of the ascidian Ciona intestinalis (L) is tadpole shaped and possesses bilateral muscle bands, a dorsal neural tube supported by an axial notochord, and sensory organs including a photoreceptive ocellus (Fig. 1A and Fig. S1A). Despite this suite of organs, the body of the Ciona larva is quite simple. The muscle band on each side lacks a segmental plan and is composed of only 18 cells arranged in a single layer (Fig. 1A and Fig. S1). The 4-5 pairs of cholinergic motor neurons located in the motor ganglion (or the visceral ganglion) have accounted for the swimming behavior (Fig. S1) (7-10). These cholinergic neurons project axons...

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Section: Resultsmentioning

confidence: 99%

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

Nishino

Baba

Okamura

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…The larva of the 'sea squirt', Ciona intestinalis (a primitive chordate rather than a true invertebrate), displays episodic irregular movements after hatching, with 5-10 s bursts of swimming occurring 3 or 4 times per minute along with shorter bursts of rapid 'tail-flicks', in trains that repeat themselves at intervals of ~15-20 min [17] . Since the larva settles and attaches to the bottom within a few hours of hatching, however, any subsequent sleep-like states would be exceedingly difficult to demonstrate.…”

Section: Ascidians (Tunicates)mentioning

confidence: 99%

Call it sleep — what animals without backbones can tell us about the phylogeny of intrinsically generated neuromotor rhythms during early development

Corner

2013

Neurosci. Bull.

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A comprehensive overview is presented of the literature dealing with the development of sleep-like motility and neuronal activity patterns in non-vertebrate animals. it has been established that spontaneous, periodically modulated, neurogenic bursts of movement appear to be a universal feature of prenatal behavior. New empirical data are presented showing that such 'seismic sleep' or 'rapid-body-movement' bursts in cuttlefish persist for some time after birth. Extensive ontogenetic research in both vertebrates and non-vertebrates is thus essential before current hypotheses about the phylogeny of motorically active sleep-like states can be taken seriously.

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“…Recent studies examining ascidian larval behavior offer insights into neural function and may also provide an assay to monitor neural dysfunction (Tsuda et al, 2003a;Meinertzhagen et al, 2004;Zega et al, 2006). One well-characterized behavior controlled by the nervous system of the ascidian tadpole larvae involves the coordinated actions guiding attachment, an event necessary for metamorphosis (Cloney, 1982).…”

Section: Transgenic Expression Of Human A 1-42 Alters Larval Behaviormentioning

confidence: 99%

“…Within 18 hours post-fertilization (hpf ), free-swimming tadpole larvae contain functional central and peripheral nervous systems that are composed of approximately 350 cells, including an anterior sensory vesicle and a visceral ganglion containing motor neurons. This simple chordate nervous system is important in coordinating several aspects of tadpole behavior, including larval swimming and their ability to respond to the environmental cues that are necessary for settlement (Zega et al, 2006;Imai and Meinertzhagen, 2007).…”

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confidence: 99%

Ascidians: an invertebrate chordate model to study Alzheimer’s disease pathogenesis

Virata

Zeller

2010

Disease Models &Amp; Mechanisms

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SUMMARY Here we present the ascidian Ciona intestinalis as an alternative invertebrate system to study Alzheimer’s disease (AD) pathogenesis. Through the use of AD animal models, researchers often attempt to reproduce various aspects of the disease, particularly the coordinated processing of the amyloid precursor protein (APP) by α-, β- and γ-secretases to generate amyloid beta (Aβ)-containing plaques. Recently, Drosophila and C. elegans AD models have been developed, exploiting the relative simplicity of these invertebrate systems, but they lack a functional Aβ sequence and a β-secretase ortholog, thus complicating efforts to examine APP processing in vivo. We propose that the ascidian is a more appropriate invertebrate AD model owing to their phylogenetic relationship with humans. This is supported by bioinformatic analyses, which indicate that the ascidian genome contains orthologs of all AD-relevant genes. We report that transgenic ascidian larvae can properly process human APP695 to generate Aβ peptides. Furthermore, Aβ can rapidly aggregate to form amyloid-like plaques, and plaque deposition is significantly increased in larvae expressing a human APP695 variant associated with familial Alzheimer’s disease. We also demonstrate that nervous system-specific Aβ expression alters normal larval behavior during attachment. Importantly, plaque formation and alterations in behavior are not only observed within 24 hours post-fertilization, but anti-amyloid drug treatment improves these AD-like pathologies. This ascidian model for AD provides a powerful and rapid system to study APP processing, Aβ plaque formation and behavioral alterations, and could aid in identifying factors that modulate amyloid deposition and the associated disruption of normal cellular function and behaviors.

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Development of swimming behaviour in the larva of the ascidianCiona intestinalis

Cited by 46 publications

References 32 publications

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

A mechanism for graded motor control encoded in the channel properties of the muscle ACh receptor

Call it sleep — what animals without backbones can tell us about the phylogeny of intrinsically generated neuromotor rhythms during early development

Ascidians: an invertebrate chordate model to study Alzheimer’s disease pathogenesis

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