Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells

Abstract

In tunicates, the coronal organ represents a sentinel checking particle entrance into the pharynx. The organ differentiates from an anterior embryonic area considered a proto-placode. For their embryonic origin, morphological features and function, coronal sensory cells have been hypothesized to be homologues to vertebrate hair cells. However, vertebrate hair cells derive from a posterior placode. This contradicts one of the principle historical criteria for homology, similarity of position, which could be taken as evidence against coronal cells/hair cells homology. In the tunicates Ciona intestinalis and C. robusta, we found that the coronal organ expresses genes (Atoh, Notch, Delta-like, Hairy-b, and Musashi) characterizing vertebrate neural and hair cell development. Moreover, coronal cells exhibit a complex synaptic connectivity pattern, and express neurotransmitters (Glu, ACh, GABA, 5-HT, and catecholamines), or enzymes for their synthetic machinery, involved in hair cell activity. Lastly, coronal cells express the Trpa gene, which encodes an ion channel expressed in hair cells. These data lead us to hypothesize a model in which competence to make secondary mechanoreceptors was initially broadly distributed through placode territories, but has become confined to different placodes during the evolution of the vertebrate and tunicate lineages.

Invaginating Structures in Synapses – Perspective

“…Interestingly, the invaginating spines of Aplysia have twice as many presynaptic vesicles as non-invaginating ones; the authors attribute this to the high degree of synaptic plasticity related to the reflex ( Bailey and Thompson, 1979 ; Bailey et al, 1979 ). Hair cell synapses of the tunicate, Ciona intestinalis , can have invaginating structures at their base and these can be postsynaptic, presynaptic, or both (reciprocal – with presynaptic vesicles on both sides of the synapse; Rigon et al, 2018 ). In the octopus ( Figure 1A ), the photoreceptor terminals form large bag- or carrot-shaped structures that are filled with presynaptic vesicles and contain (1) invaginating postsynaptic spines, (2) presynaptic vesicle-filled “finger twigs” from adjacent carrots, and (3) “tunnel fibers” from small neurons ( Dilly et al, 1963 ; Case et al, 1972 ).…”

Diversity of cilia-based mechanosensory systems and their functions in marine animal behaviour

“…Coronal cells in ascidians share a regulatory geneexpression signature with vertebrate hair cells and express the TRP channel TRPA, but not TRPN [78]. Whether TRPA is important for mechanosensation in the tunicate coronal cells is not known.…”

Comparative Neurobiology of Biogenic Amines in Animal Models in Deuterostomes

“…Interestingly, by analyzing TPH expression in adult C. robusta, serotonergic neurons have also been found in the tentacle of coronal cells in the oral siphon. These cells are homologous to vertebrate hair cells (Rigon et al, 2018).…”

“…In adult C. robusta, components of the catecholaminergic pathway, such as tyrosine hydroxylase, occur in coronal cells within the oral siphon tentacles (Rigon et al, 2018). Dopamine localization in coronal cells could play a protective role on the nerve synapse, given the homology of these cells to mammalian hair cells, for which it acts likewise (Lendvai et al, 2011).…”