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Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire [1]

['Athira Athira', 'Sars International Centre For Marine Molecular Biology', 'University Of Bergen', 'Bergen', 'Daniel Dondorp', 'Jerneja Rudolf', 'Olivia Peytral', 'Marios Chatzigeorgiou']

Date: 2022-08 

Vertebrate nervous systems can generate a remarkable diversity of behaviors. However, our understanding of how behaviors may have evolved in the chordate lineage is limited by the lack of neuroethological studies leveraging our closest invertebrate relatives. Here, we combine high-throughput video acquisition with pharmacological perturbations of bioamine signaling to systematically reveal the global structure of the motor behavioral repertoire in the Ciona intestinalis larvae. Most of Ciona’s postural variance can be captured by 6 basic shapes, which we term “eigencionas.” Motif analysis of postural time series revealed numerous stereotyped behavioral maneuvers including “startle-like” and “beat-and-glide.” Employing computational modeling of swimming dynamics and spatiotemporal embedding of postural features revealed that behavioral differences are generated at the levels of motor modules and the transitions between, which may in part be modulated by bioamines. Finally, we show that flexible motor module usage gives rise to diverse behaviors in response to different light stimuli.

Data Availability: We have established a repository containing datasets corresponding to this study. Specifically, it contains 1. Multi-point tracking data of the larvae obtained using the Tierpsy Tracker (skeletons) 2. Features like curvature, speed, etc calculated from the tracking data 3. The results of time-series analyses approaches (matrix profiling, HMM, Spatio-temporal clustering) performed on the feature dataset. 4. The Hidden Markov Models trained for inferences The link to the zenodo repository is: https://zenodo.org/record/6761772#.YrsDNexBxyF The DOI for these datasets is: 10.5281/zenodo.6761772 Code for acquisition software can be found here: https://github.com/ChatzigeorgiouGroup/imMobilize Notebooks for Matrix profiling analysis is available here: https://github.com/ChatzigeorgiouGroup/ciona_behaviour_matrix_profile Code for biophysical features, HMM, spatio-temporal embedding and statistical analysis: https://github.com/ChatzigeorgiouGroup/behavior_ciona_bioamines .

In this work, we address this knowledge gap by using machine vision to track, skeletonize, and extract postural features from thousands of larvae swimming both spontaneously and under light stimulation. We additionally combine wild-type swimming behavioral analysis with a small-scale pharmacobehavioral screen that targets bioamine signaling, a key regulator of the biophysical properties of neurons, synapses [ 30 , 35 , 36 ], and behavior [ 30 , 37 ]. Using dimensionality reduction, we derive lower dimensional representations of body postures, which we term “eigencionas.” With these, we can explain the majority of postural variance in the Ciona larvae. We also combine 3 state-of-the-art approaches: motif identification, hidden Markov model (HMM), and spatiotemporal embedding to quantitatively define Ciona larval behavioral dynamics and thereby uncover the perturbation-sensitive modulation effects exerted on them by bioamine neuromodulators.

Invertebrate chordates belonging to the phylum Chordata are obvious candidates for neuroethological analysis since they are close relatives of vertebrates and may provide important insight into the evolution of chordate nervous systems. While the importance of studying invertebrate chordates has been recognized in the field of evo-devo, as evident from an explosion of evolutionary, genomic, and developmental studies primarily in 3 organisms: the cephalochordate amphioxus and the tunicates Ciona intestinalis and Oikopleura dioica, these organisms have yet to be leveraged in the context of neuroscience. Understanding their nervous system functions and behavioral repertoire will provide insights into the conservation and diversity of locomotory circuits and how these relate to the evolution of the diverse modes of locomotor behavior [ 20 ].

A primary function of animal nervous system is to transform sensory input into a sequence of actions known as behavioral output. Thus, the overarching motive of neurobiology research is to delineate the functional makeup and mechanistic basis of these behavioral outputs. Major progress has relied on the development of experimental tools and analysis methods that permit real time measurements and quantitative characterization of behavior (reviewed in [ 1 – 5 ]). Among the various natural animal behaviors, locomotion forms an integral part of nervous system function. Researchers in the field have been able to employ the aforementioned modern technologies to define motor actions as a function of their natural stereotyped elements, known as behavioral “modules,” “motifs,” “syllables,” or “primitives” [ 1 , 6 – 10 ], where these basic building blocks of motor behavior operate under organizational and hierarchical rules that bear similarities to phonological and syntactical rules that govern language. Modern systems neuroscience approaches have greatly facilitated the investigation of vertebrate motor modules [ 11 – 13 ], which in invertebrates are even more likely to be interrogated with high sensitivity and precision, largely due to the latter’s smaller nervous systems [ 14 – 16 ]. In addition, the next generation of neuroscience discovery capitalizes on developing and studying new nontraditional model species to reveal not only common principles, but also differences in behavioral organization across the tree of life as well as within important clades [ 17 – 19 ]. Consequently, there is an urgent requirement for expanding neuroethological studies to additional organisms occupying key phylogenetic positions.

Results

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001744

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