Abstract

Many spinal circuits dedicated to locomotor control have been identified in the developing zebrafish. How these circuits operate together to generate the various swimming movements during development remains to be clarified. In this study, we iteratively built models of developing zebrafish spinal circuits coupled to simplified musculoskeletal models that reproduce coiling and swimming movements. The neurons of the models were based upon morphologically or genetically identified populations in the developing zebrafish spinal cord. We simulated intact spinal circuits as well as circuits with silenced neurons or altered synaptic transmission to better understand the role of specific spinal neurons. Analysis of firing patterns and phase relationships helped to identify possible mechanisms underlying the locomotor movements of developing zebrafish. Notably, our simulations demonstrated how the site and the operation of rhythm generation could transition between coiling and swimming. The simulations also underlined the importance of contralateral excitation to multiple tail beats. They allowed us to estimate the sensitivity of spinal locomotor networks to motor command amplitude, synaptic weights, length of ascending and descending axons, and firing behavior. These models will serve as valuable tools to test and further understand the operation of spinal circuits for locomotion.

Highlights

  • Movements made in the early stages of development can be critical for the survival of many species

  • We aimed to model how new locomotor movements may emerge from the integration of spinal interneurons and the modification of synaptic weights and firing behaviour over the first few days of development in the zebrafish

  • The composition of each model depended on the developmental stage and the locomotor movement to be generated. 133 Single coiling (> 17 hpf) results from unilateral gap junction coupling Coiling, which is already observed at 1 dpf, is characterized by a single strong, slow tail beat on one side of the body followed by a return to resting position (Saint-Amant & Drapeau, 1998)

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Summary

Introduction

Movements made in the early stages of development can be critical for the survival of many species. 78 During this rapid series of transitions between locomotor maneuvers, populations of spinal neurons are progressively generated, starting with primary motoneurons at about 9 hpf. The first wave occurs around 16-17 hpf It includes axon growth in primary motoneurons (MNs) that innervate red and white muscle fibres at early developmental stages (Buss & Drapeau, 2000). The progressive generation of new populations of spinal neurons and continued axonal growth coincides with the expansion of the zebrafish locomotor repertoire. This timing suggests that incorporating spinal circuits into existing locomotor circuits underlies the acquisition of novel locomotor maneuvers

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