Abstract
The spinal locomotor network is frequently used for studies into how neuronal circuits are formed and how cellular activity shape behavioral patterns. A population of dI6 interneurons, marked by the Doublesex and mab-3 related transcription factor 3 (Dmrt3), has been shown to participate in the coordination of locomotion and gaits in horses, mice and zebrafish. Analyses of Dmrt3 neurons based on morphology, functionality and the expression of transcription factors have identified different subtypes. Here we analyzed the transcriptomes of individual cells belonging to the Dmrt3 lineage from zebrafish and mice to unravel the molecular code that underlies their subfunctionalization. Indeed, clustering of Dmrt3 neurons based on their gene expression verified known subtypes and revealed novel populations expressing unique markers. Differences in birth order, differential expression of axon guidance genes, neurotransmitters, and their receptors, as well as genes affecting electrophysiological properties, were identified as factors likely underlying diversity. In addition, the comparison between fish and mice populations offers insights into the evolutionary driven subspecialization concomitant with the emergence of limbed locomotion.
Highlights
Locomotor behaviors are coordinated by subsets of excitatory and inhibitory interneurons in the spinal cord that form a central pattern generator (CPG)
Spinal tissue, collected to prevent inclusion of the hind brain, brain stem, and the most caudal part of the spinal cord was used for fluorescence assisted cell sorting (FACS). eGFP positive neurons from dmrt3a:Gal4;UAS:eGFP transgenic zebrafish at 3 days post fertilization and tdTomato positive neurons from embryonic day 14.5 (E14.5) Dmrt3Cre:tdTomato mice were sorted and collected into 384 well plates (Figure 1A)
This led to the identification of an additional dmrt3a/dI6 cluster of cells that were retained for downstream analysis
Summary
Locomotor behaviors are coordinated by subsets of excitatory and inhibitory interneurons in the spinal cord that form a central pattern generator (CPG). These neurons coordinate movements at different locomotor speeds by dictating the recruitment pattern and output frequency of motor neurons (Boije and Kullander, 2018). The locomotor CPG has been widely studied since it allows for analysis of a relatively simple neuronal circuit with a clear functional output. Twelve progenitor domains have been defined along the dorso-ventral axis of the mouse spinal cord that differentiate into 23 subtypes of neurons (Lu et al, 2015). Studies of interneurons in mice illustrate the vast heterogeneity that exists within defined populations, as combinatorial antibody labeling revealed at least 50
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