A GABAergic Maf-expressing interneuron subset regulates the speed of locomotion in Drosophila

J Valmier,A Garcès,P Carroll,S Yoshikawa,M F Zwart,J B Thomas,J Enriquez,T Jovanic,C Surel,H Babski

doi:10.1038/s41467-019-12693-6

Abstract

Interneurons (INs) coordinate motoneuron activity to generate appropriate patterns of muscle contractions, providing animals with the ability to adjust their body posture and to move over a range of speeds. In Drosophila larvae several IN subtypes have been morphologically described and their function well documented. However, the general lack of molecular characterization of those INs prevents the identification of evolutionary counterparts in other animals, limiting our understanding of the principles underlying neuronal circuit organization and function. Here we characterize a restricted subset of neurons in the nerve cord expressing the Maf transcription factor Traffic Jam (TJ). We found that TJ+ neurons are highly diverse and selective activation of these different subtypes disrupts larval body posture and induces specific locomotor behaviors. Finally, we show that a small subset of TJ+ GABAergic INs, singled out by the expression of a unique transcription factors code, controls larval crawling speed.

Highlights

Interneurons (INs) coordinate motoneuron activity to generate appropriate patterns of muscle contractions, providing animals with the ability to adjust their body posture and to move over a range of speeds
We found that two of the three Traffic Jam (TJ)+ GABAergic midline cells belong to the median neuroblast (MNB) progeny subpopulation identified by nuclear Pros expression (Pros-nucl)[31] (Fig. 9a, double empty arrowheads)
We found that all three TJ+ GABAergic cells are forkhead+ and Engrailed+ (En+) (Fig. 9d, e; full arrowheads), two transcription factors (TFs) known to be expressed in a subpopulation of MNB progeny, and iVUMs31

Summary

Introduction

Interneurons (INs) coordinate motoneuron activity to generate appropriate patterns of muscle contractions, providing animals with the ability to adjust their body posture and to move over a range of speeds. The rhythmic bursts of MN activity are controlled by local excitatory and inhibitory interneurons (INs) located in the ventral region of the vertebrate spinal cord and in the ventral nerve cord (VNC) of invertebrates These INs can be grouped into subclasses on the basis of their connectivity patterns, physiological properties such as neurotransmitter used, and by the set of specific transcription factors (TFs) they express. Using transgenic lines and intersectional genetics, one can precisely control the expression of ion channel proteins and regulate IN activity[7,8] Such an approach has proved instrumental in dissecting the core logic of the CPG circuits that generate the rhythm and pattern of motor output in both vertebrates and in Drosophila[3,5,9]. We provide evidence that these MNB progeny neurons belong to the recently characterized Ladder neurons, a subtype of feedforward inhibitory INs that mediate behavioral choice during mechanosensory responses in the larva 17

Methods

Results

Conclusion