Comprehensive analysis of behavioral dynamics in the protochordateCiona intestinalis

Abstract

Locomotion is broadly conserved in the animal kingdom, yet our understanding of how complex locomotor behaviors are generated and have evolved is relatively limited by the lack of an accurate description of their structural organization. Here we take a neuroethological approach to break down the motor behavioral repertoire of one of our nearest invertebrate relative, the protochordate Ciona intestinalis, into basic building blocks. Using machine vision, we track thousands of swimming larvae to obtain a feature-rich description of larval swimming and show that most of the postural variance can be captured by six basic shapes, which we term “Eigencionas”. Using multiple complementary approaches, we built representations of the larval behavioral dynamics and systematically reveal the global structure of behavior. By employing matrix profiling and subsequence time-series clustering, we reveal that Ciona swimming is rich in stereotyped behavioral motifs. Combining pharmacological inhibition of bioamine signaling with Hidden Markov Model we discover underlying behavioral states including multiple modes of roaming and dwelling. Finally, performing a spatio-temporal embedding of the postural features onto a behavioral space provides insight into the behavioral repertoire by project it to a low-dimensional space and highlights subtle light stimulus evoked behavioral differences.Taken together, Ciona larvae generate their spontaneous swimming and visuomotor behavioral repertoire by altering both their motor modules and transitions between, which are amenable to pharmacological perturbations, facilitating future functional and mechanistic investigations.

Sensory cells in tunicates: insights into mechanoreceptor evolution

“…For instance, mechanical stimulation of the adhesive/sensory papillae, the three sensory organs (two dorsal and one ventral) located in the anterior larval region (Figures 1E, 2A-B) is sufficient and necessary to trigger metamorphosis in Ciona (Wakai et al, 2021;Sakamoto et al, 2022). While mechanosensitive modulation of swimming has yet to be definitively shown in ascidian larvae, startle-like behaviors have been described in Ciona (Athira et al, 2022). Here we discuss what is known about the development and function of the candidate primary mechanosensory cell types that have been identified in these larvae.…”

Transitions of motor neuron activities during Ciona development

“…Recent research revealed that ascidian larvae exhibit multiple types of swimming, and their tail curvature varies depending on the stimulus. (Athira et al, 2022;McHenry, 2001;Nishino et al, 2011). Further analysis and fine tuning of DeepLabCut training data might be required to analyze the correlation between Ca 2+ oscillations and these various types of swimming in detail.…”

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

“…intestinalis a marine invertebrate chordate that belongs to the sister group of vertebrates 12,13 and has a biphasic cycle which entails a tadpole-shaped, freely swimming larva which undergoes metamorphosis to generate the filter feeding adult [14][15][16][17][18] . C. intestinalis larvae possess a small optically accessible nervous system suitable for functional imaging 19 , with a fully mapped synaptic connectome 20,21 , which generates a rich behavioral repertoire 22 making them an ideal system for studying the sensory mechanisms underlying attachment, settlement, and metamorphosis of marine larvae. Previous studies have provided a detailed description of the morphogenetic steps that take place during settlement and metamorphosis over the course of a few hours 14,17,18 .…”