Behavioural characterization of dmrt3a mutant zebrafish reveals crucial aspects of vertebrate locomotion through phenotypes related to acceleration

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Vertebrate locomotion is orchestrated by spinal interneurons making up a central pattern generator. Proper coordination of activity, both within and between segments, is required to generate the desired locomotor output. This coordination is altered during acceleration to ensure the correct recruitment of muscles for the chosen speed. The transcription factor Dmrt3 has been proposed to shape the patterned output at different gaits in horses and mice. Here, we characterized dmrt3a mutant zebrafish, which showed a strong, transient, locomotor phenotype in developing larvae. During beat-and-glide swimming, mutant larvae showed fewer and shorter movements with decreased velocity and acceleration. Developmental compensation likely occurs as the analysed behaviours did not differ from wild type at older larval stages. However, analysis of maximum swim speed in juveniles suggests that some defects persists within the mature locomotor network of dmrt3a mutants. Our results reveal the pivotal role Dmrt3 neurons play in shaping the patterned output during acceleration in vertebrates.

Significance statement This study shows that dmrt3a expressing spinal neurons are crucial for coordinating locomotion in fish, a function that must have arisen early during the evolution of vertebrates. Analyses of two dmrt3a mutant zebrafish lines, one similar to the “gait-keeper” mutation in horses and one similar to the null mutant in mice, allow us to evaluate differences in locomotor phenotypes within a single species. Characterization throughout development gives insights into the fundamental role these interneurons play to establish coordinated locomotion. Our results suggest that zebrafish is an excellent model to reveal how speed changes are orchestrated in vertebrates by examining the activity of dmrt3a expressing interneurons in vivo at a cellular level in relation to acceleration.

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