Investigating the role of low level reinforcement reflex loops in insect locomotion

Abstract

Insects are highly capable walkers, but many questions remain regarding how the insect nervous system controls locomotion. One particular question is how information is communicated between the ‘lower level’ ventral nerve cord (VNC) and the ‘higher level’ head ganglia to facilitate control. In this work, we seek to explore this question by investigating how systems traditionally described as ‘positive feedback’ may initiate and maintain stepping in the VNC with limited information exchanged between lower and higher level centers. We focus on the ‘reflex reversal’ of the stick insect femur-tibia joint between a resistance reflex (RR) and an active reaction in response to joint flexion, as well as the activation of populations of descending dorsal median unpaired (desDUM) neurons from limb strain as our primary reflex loops. We present the development of a neuromechanical model of the stick insect (Carausius morosus) femur-tibia (FTi) and coxa-trochanter joint control networks ‘in-the-loop’ with a physical robotic limb. The control network generates motor commands for the robotic limb, whose motion and forces generate sensory feedback for the network. We based our network architecture on the anatomy of the non-spiking interneuron joint control network that controls the FTi joint, extrapolated network connectivity based on known muscle responses, and previously developed mechanisms to produce ‘sideways stepping’. Previous studies hypothesized that RR is enacted by selective inhibition of sensory afferents from the femoral chordotonal organ, but no study has tested this hypothesis with a model of an intact limb. We found that inhibiting the network’s flexion position and velocity afferents generated a reflex reversal in the robot limb’s FTi joint. We also explored the intact network’s ability to sustain steady locomotion on our test limb. Our results suggested that the reflex reversal and limb strain reinforcement mechanisms are both necessary but individually insufficient to produce and maintain rhythmic stepping in the limb, which can be initiated or halted by brief, transient descending signals. Removing portions of this feedback loop or creating a large enough disruption can halt stepping independent of the higher-level centers. We conclude by discussing why the nervous system might control motor output in this manner, as well as how to apply these findings to generalized nervous system understanding and improved robotic control.