Synchronous multi-segmental activity between metachronal waves controls locomotion speed in Drosophila larvae

Abstract

The ability to adjust the speed of locomotion is essential for survival. In limbed animals, the frequency of locomotion is modulated primarily by changing the duration of the stance phase. The underlying neural mechanisms of this selective modulation remain an open question. Here, we report a neural circuit controlling a similarly selective adjustment of locomotion frequency in Drosophila larvae. Drosophila larvae crawl using peristaltic waves of muscle contractions. We find that larvae adjust the frequency of locomotion mostly by varying the time between consecutive contraction waves, reminiscent of limbed locomotion. A specific set of muscles, the lateral transverse (LT) muscles, co-contract in all segments during this phase, the duration of which sets the duration of the interwave phase. We identify two types of GABAergic interneurons in the LT neural network, premotor neuron A26f and its presynaptic partner A31c, which exhibit segmentally synchronized activity and control locomotor frequency by setting the amplitude and duration of LT muscle contractions. Altogether, our results reveal an inhibitory central circuit that sets the frequency of locomotion by controlling the duration of the period in between peristaltic waves. Further analysis of the descending inputs onto this circuit will help understand the higher control of this selective modulation.

Specific presynaptic functions require distinct Drosophila Cav2 splice isoforms

“…Although crawling speed of Drosophila larvae is mainly adjusted by varying the duration between subsequent peristaltic waves of motoneuron bursting (peristaltic wave period duration, Liu et al 2023), differences in Ca v 2 mediated neuromuscular synaptic transmission may also play an important role. In accordance with reduced charge transfer to the postsynaptic muscle cell upon excision of the I-IIB exon (Figs.…”

Modular organization of synapses within a neuromere for distinct axial locomotion inDrosophilalarvae

“…Calcium imaging assay demonstrates that the AL domains do not exhibit direction-independent activity recruitment with the PI domains (Figure 4A-4B). Since the contraction of transverse muscles during crawling depends on experimental conditions (32), the function of AIc activity is still unclear. Further connectomics and functional analysis of the PI and AIc domains will clarify the roles of direction-independent domains in motor control.…”

“…Calcium imaging assay demonstrates that the AL domains do not exhibit direction-independent activity recruitment with the PI domains (Figure 4A-4B). Since the contraction of transverse muscles during crawling depends on experimental conditions (32), the function of AIc activity is still unclear.…”