Polymodal sensory perception of mechanical and chemical cues drives robust settlement and metamorphosis of a marine pre-vertebrate zooplanktonic larva

Abstract

The Earth's oceans brim with an incredible diversity of microscopic planktonic animals, many of which correspond to the transient larval stage in the life cycles of benthic marine organisms. The mechanisms by which marine larvae use their nervous system to sense and process diverse environmental cues (physical and chemical) in the water column and the benthos to settle and metamorphose is a major problem across the fields of neuroscience, development, evolution and ecology, yet they remain largely unclear. Here, we employ Ca2+ imaging and behavioral assays using the larval form of the protochordate Ciona intestinalis to characterise the mechanical and chemical stimuli these larvae respond to during settlement and metamorphosis. We also identify the polymodal sensory cells that detect these stimuli. Whole brain Ca2+ imaging further revealed that the presentation or removal of ethological chemosensory stimuli engages the activities of different neuronal sub-populations resulting in brain state changes, which may underlie behavioral action selections and metamorphosis. Finally, chemogenetic interrogation coupled to behavioral analysis reveals that peptidergic sensory neurons including polymodal cells capable of chemotactile perception and chemosensory/neurosecretory cells of proto-placodal ectoderm origin play a pivotal role in regulating stimulus induced settlement and metamorphosis. This work suggests that marine zooplanktonic larvae utilise their streamlined nervous systems to perform multimodal integration of ethologically physical and chemical cues to explore the oceanic water column and benthos.

Using CRISPR/Cas9 to identify genes required for mechanosensory neuron development and function

“…The requirement of Vamp1/2/3 for papilla neuron-mediated tail retraction is not surprising, given its central role in synaptic transmission. Recent studies have demonstrated that mechanosensory papilla neuron activity is necessary for tail retraction and metamorphosis in Ciona ( Hoyer et al, 2023 preprint; Sakamoto et al, 2022 ; Wakai et al, 2021 ). While the papilla neurons are glutamatergic, additional neurotransmitters have been implicated in metamorphosis, including noradrenaline ( Kimura et al, 2003 ), GABA, and gonadotropin-releasing hormone ( Hozumi et al, 2020 ).…”

Specification of distinct cell types in a sensory-adhesive organ important for metamorphosis in tunicate larvae

“…Besides adhesion, a key role of the papilla is to act as an organ for bimodal mechano- and chemo-sensation regulating larval settlement and metamorphosis [ 75 ]. It has been proposed that the papilla territory may be a homolog of the olfactory placode, based on the expression of several regulators investigated in this study including Sp6/7/8 , Islet , Foxc , and Foxg [ 18 , 21 ].…”