Selective Inhibition Mediates the Sequential Recruitment of Motor Pools

Maarten F Zwart,Stefan R Pulver,James W Truman,Akira Fushiki,Richard D Fetter,Albert Cardona,Matthias Landgraf

doi:10.1016/j.neuron.2016.06.031

Abstract

SummaryLocomotor systems generate diverse motor patterns to produce the movements underlying behavior, requiring that motor neurons be recruited at various phases of the locomotor cycle. Reciprocal inhibition produces alternating motor patterns; however, the mechanisms that generate other phasic relationships between intrasegmental motor pools are unknown. Here, we investigate one such motor pattern in the Drosophila larva, using a multidisciplinary approach including electrophysiology and ssTEM-based circuit reconstruction. We find that two motor pools that are sequentially recruited during locomotion have identical excitable properties. In contrast, they receive input from divergent premotor circuits. We find that this motor pattern is not orchestrated by differential excitatory input but by a GABAergic interneuron acting as a delay line to the later-recruited motor pool. Our findings show how a motor pattern is generated as a function of the modular organization of locomotor networks through segregation of inhibition, a potentially general mechanism for sequential motor patterns.

Highlights

Movements are generated by precise sequences of activity in motor systems
Our results show that the segregation of input onto distinct intrasegmental motor neurons facilitates the generation of a widespread motor pattern through selective inhibition of a motor pool
The longitudinal muscles, running parallel to the length of the animal, begin to contract before transverse muscles, which are oriented perpendicular to the main body axis (Heckscher et al, 2012; Figures 1A and 1B). This is followed by a period of co-contraction of both muscle sets (Figures 1A and 1B). This intrasegmental muscle contraction sequence is unlike alternating left-right or flexorextensor activation, which has been a primary focus of studies in vertebrate model systems (Kiehn, 2011)

Summary

Introduction

In spite of decades of research, the logic underlying the neural circuitry that produces these sequences during locomotion remains unclear (Buschges et al, 2011; Harris and Weinberg, 2012; McLean and Dougherty, 2015) Attempts to decipher this logic have largely focused on the alternating patterns of activity that underlie the recruitment of antagonistic motor units, such as flexors and extensors (Grillner, 2003; Grillner and Jessell, 2009; McLean and Dougherty, 2015; Talpalar et al, 2011; Tripodi et al, 2011), depressors and elevators (Burrows, 1996), and the bilaterally homologous motor units that generate left-right alternation (Grillner, 2003; Talpalar et al, 2013). In spite of the prominence of this type of motor pattern, it is unknown how premotor circuits generate the required sequential patterns of activity within each segment in the appropriate motor neurons

Results

Discussion

Conclusion