Abstract
Left-right asymmetries in brains are usually minor or cryptic. We report brain asymmetries in the tiny, dorsal tubular nervous system of the ascidian tadpole larva, Ciona intestinalis. Chordate in body plan and development, the larva provides an outstanding example of brain asymmetry. Although early neural development is well studied, detailed cellular organization of the swimming larva's CNS remains unreported. Using serial-section EM we document the synaptic connectome of the larva's 177 CNS neurons. These formed 6618 synapses including 1772 neuromuscular junctions, augmented by 1206 gap junctions. Neurons are unipolar with at most a single dendrite, and few synapses. Some synapses are unpolarised, others form reciprocal or serial motifs; 922 were polyadic. Axo-axonal synapses predominate. Most neurons have ciliary organelles, and many features lack structural specialization. Despite equal cell numbers on both sides, neuron identities and pathways differ left/right. Brain vesicle asymmetries include a right ocellus and left coronet cells.
Highlights
IntroductionAnimals exhibit various forms of left-right asymmetry (Ludwig, 1932; Neville, 1976; Brown and Wolpert, 1990; Palmer, 2009), and anatomical examples in brains are reported both in invertebrates (Hobert et al, 2002; Frasnelli et al, 2012), and vertebrates (Rogers and Andrew, 2002; Duboc et al, 2015) as differences in cell number (Blinkov and Glezer, 1968, their tables 184 and 185) and in the lateralization of the mammalian cortex (Galaburda et al, 1978)
A total of 3375 60 nm sections that started at the level of the otolith pigment and extended to the posterior motor ganglion, followed by 1360 70 nm sections cut into the anterior tail, and continued to its tip by a further 2193 100 nm sections (Figure 1; Figure 1—figure supplement 1) were collected and imaged at 3.85 nm per pixel
We report the full synaptic connectome of a single tadpole larva of a model chordate species, the ascidian Ciona intestinalis, and use this to identify the complete inventory of the many asymmetrical features in its central nervous system (CNS)
Summary
Animals exhibit various forms of left-right asymmetry (Ludwig, 1932; Neville, 1976; Brown and Wolpert, 1990; Palmer, 2009), and anatomical examples in brains are reported both in invertebrates (Hobert et al, 2002; Frasnelli et al, 2012), and vertebrates (Rogers and Andrew, 2002; Duboc et al, 2015) as differences in cell number (Blinkov and Glezer, 1968, their tables 184 and 185) and in the lateralization of the mammalian cortex (Galaburda et al, 1978). The CNS forms from a neural tube, yet exhibits left/right differences, and so provides a useful model to study many aspects of brain asymmetry. This issue is important because brain laterality has been associated with increased fitness for animal life (Duboc et al, 2015)
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