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Abstract
BackgroundLeft-right asymmetries are a common feature of metazoans and can be found in a number of organs including the nervous system. These asymmetries are particularly pronounced in the simple central nervous system (CNS) of the swimming tadpole larva of the tunicate Ciona, which displays a chordate ground plan. While common pathway elements for specifying the left/right axis are found among chordates, particularly a requirement for Nodal signaling, Ciona differs temporally from its vertebrate cousins by specifying its axis at the neurula stage, rather than at gastrula. Additionally, Ciona and other ascidians require an intact chorionic membrane for proper left-right specification. Whether such differences underlie distinct specification mechanisms between tunicates and vertebrates will require broad understanding of their influence on CNS formation. Here, we explore the consequences of disrupting left-right axis specification on Ciona larval CNS cellular anatomy, gene expression, synaptic connectivity, and behavior.ResultsWe show that left-right asymmetry disruptions caused by removal of the chorion (dechorionation) are highly variable and present throughout the Ciona larval nervous system. While previous studies have documented disruptions to the conspicuously asymmetric sensory systems in the anterior brain vesicle, we document asymmetries in seemingly symmetric structures such as the posterior brain vesicle and motor ganglion. Moreover, defects caused by dechorionation include misplaced or absent neuron classes, loss of asymmetric gene expression, aberrant synaptic projections, and abnormal behaviors. In the motor ganglion, a brain structure that has been equated with the vertebrate hindbrain, we find that despite the apparent left-right symmetric distribution of interneurons and motor neurons, AMPA receptors are expressed exclusively on the left side, which equates with asymmetric swimming behaviors. We also find that within a population of dechorionated larvae, there is a small percentage with apparently normal left-right specification and approximately equal population with inverted (mirror-image) asymmetry. We present a method based on a behavioral assay for isolating these larvae. When these two classes of larvae (normal and inverted) are assessed in a light dimming assay, they display mirror-image behaviors, with normal larvae responding with counterclockwise swims, while inverted larvae respond with clockwise swims.ConclusionsOur findings highlight the importance of left-right specification pathways not only for proper CNS anatomy, but also for correct synaptic connectivity and behavior.
Highlights
Left-right asymmetries are a common feature of metazoans and can be found in a number of organs including the nervous system
We show here that the disruptions to left-right asymmetry caused by dechorionation extend beyond the sensory systems and are observed throughout the length of the larval central nervous system (CNS)
The previously undescribed left-right asymmetries described here for Ciona larval CNS anatomy, gene expression, synaptic projections, and behavior all are disrupted by early dechorionation, suggesting they are driven by the common mechanism, despite being highly variable
Summary
Left-right asymmetries are a common feature of metazoans and can be found in a number of organs including the nervous system These asymmetries are pronounced in the simple central nervous system (CNS) of the swimming tadpole larva of the tunicate Ciona, which displays a chordate ground plan. Ciona larvae have two distinct visuomotor behaviors, negative phototaxis and a looming shadow response, that are mediated by separate groups of photoreceptors, the Group I and Group II clusters, respectively [10]. Both visuomotor circuits act via minimal circuits that consist of two-interneuron sequences. The antenna cells (Fig. 1) sense the movement of the otolith pigment cell as the larva moves with respect to gravity, but the targets of the antenna cell in the pBV, the antenna relay neurons, are inhibited by photoreceptor RNs, unless the larva sees a light dim, at which point the inhibition is released and the larva swims upwards [8]
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