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Divergence of exploratory locomotion and the underlying neuronal circuitry in two closely related vertebrate species

Abstract : Walking, swimming, hopping and crawling –– are only a few examples of the diverse forms of locomotion in nature. Locomotion is adapted to the environmental constraints of an animal. In this thesis, I established an approach to understand how neuronal circuits underlying locomotion diverge in nature by compar¬ing larvae of two closely related species that occupy similar environments and exhibit different swimming behaviors. The classical genetic model organism Danio rer¬io or zebrafish (ZF) and the closely related Danionin species Danionella translucida (DT) were used in the study. I investigated the proximate (cellular and physiological) and ultimate (organismal) causes behind this divergence in swimming behavior despite the phylogenetic and environmental proximity that the two species share.To examine the swimming behavior in the two fishes, I developed a high-speed imaging system and an analysis pipeline. The swims were broken down into half tail beats to be able to probe comparable units of locomotion in the two species. The analysis showed that during spontaneous swimming, the DT larvae utilize lower tail-beat frequencies and lower tail angles to execute slower yet longer swim events. In comparison, the ZF larvae execute a fast and intermittent “burst-and-glide” swimming. However, during escapes, DT can attain high maximum speeds with the latency to the maximum speed being surprisingly lower than that of ZF. In spontaneously swimming fish, despite the large differences in the instantaneous speeds, the mean squared displacement was found to be comparable between the two animals. This is due to a slower randomization of orientation in DT compared to ZF which leads to a longer ballistic swimming regime in DT. In addition to the characterization of the fine structure of the swimming and the influence of the swimming pattern on exploration, from an organismal perspective, I proposed two observations – a lower availability of dissolved oxygen to DT due to its preference to the bottom layers of water column and a delayed inflation of swim bladder in DT – as factors contributing to the observed swimming pattern in DT.Using in-situ hybridization and immunohistochemistry, a high degree of similarity is shown in the distribution of excitatory and inhibitory neurons in the hindbrain. Moreover, based on backfill experiments, a strong conservation is observed in the distribution of reticulospinal neurons projecting from the brainstem to the spinal cord. To probe the physiological differences, I created a DT Tg(HuC:H2B-GCaMP6s), a transgenic DT with near pan-neuronal nucleus-localized expression of genetically encoded calcium indicator GCaMP6s. Using this transgenic DT and an equivalent transgenic ZF, I carried out light sheet imaging in spontaneously swimming DT and ZF. With this approach, we identified neuronal populations in the DT brain that scaled their activity with the increased swimming activity in DT. These regions are potential candidates for providing an excitatory drive to the downstream neurons to keep the central pattern generators in the spinal cord active to produce a long continuous swimming. Furthermore, the long swim events in DT allowed a further dissection of the swimming correlated neurons with respect to different phases of the swimming.In conclusion, the work provides a unique insight, from a behavioral and physiological perspective, into the ability of similar neuronal circuits to produce different behavioral outputs. The results were also briefly evaluated from an organismal viewpoint. To our knowledge, such a comprehensive comparison, combining behavior, anatomy and physiology has not been carried out directly between two vertebrate animals before. This work also lays a foundation for future comparative studies in vertebrate neuroscience, especially among Danionins, to gain a thorough understanding of neuronal circuits underlying behaviors.
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Submitted on : Saturday, January 1, 2022 - 1:14:43 AM
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Gokul Rajan. Divergence of exploratory locomotion and the underlying neuronal circuitry in two closely related vertebrate species. Neurons and Cognition [q-bio.NC]. Université Paris sciences et lettres, 2020. English. ⟨NNT : 2020UPSLT010⟩. ⟨tel-03505902⟩



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