A locomotor neural circuit persists and functions similarly in larvae and adult Drosophila.

Kristen Lee,Chris Q Doe

doi:10.7554/elife.69767

Abstract

Individual neurons can undergo drastic structural changes, known as neuronal remodeling or structural plasticity. One example of this is in response to hormones, such as during puberty in mammals or metamorphosis in insects. However, in each of these examples, it remains unclear whether the remodeled neuron resumes prior patterns of connectivity, and if so, whether the persistent circuits drive similar behaviors. Here, we utilize a well-characterized neural circuit in the Drosophila larva: the moonwalker descending neuron (MDN) circuit. We previously showed that larval MDN induces backward crawling, and synapses onto the Pair1 interneuron to inhibit forward crawling (Carreira-Rosario et al., 2018). MDN is remodeled during metamorphosis and regulates backward walking in the adult fly. We investigated whether Pair1 is remodeled during metamorphosis and functions within the MDN circuit during adulthood. We assayed morphology and molecular markers to demonstrate that Pair1 is remodeled during metamorphosis and persists in the adult fly. MDN-Pair1 connectivity is lost during early pupal stages, when both neurons are severely pruned back, but connectivity is re-established at mid-pupal stages and persist into the adult. In the adult, optogenetic activation of Pair1 resulted in arrest of forward locomotion, similar to what is observed in larvae. Thus, the MDN-Pair1 neurons are an interneuronal circuit - a pair of synaptically connected interneurons - that is re-established during metamorphosis, yet generates similar locomotor behavior at both larval and adult stages.

Highlights

Large-scale changes in neuronal morphology and function occur during mammalian puberty (Barendse et al., 2018; Mills et al, 2016; Sisk and Zehr, 2005), as well as several neurobiological disorders including depression (Patel et al, 2019), or chronic pain (Kuner and Flor, 2017)
We follow our previous work showing that Moonwalking Descending Neuron (MDN) is remodeled during metamorphosis and persists into the adult (Carreira-Rosario et al, 2018) by asking: Is the MDN partner neuron Pair1 maintained in the adult? Does the adult Pair1 induce an inhibition in forward locomotion, similar to its role in larvae? And, are the adult Pair1 and MDN synaptically coupled? We find that all of these questions are answered in the affirmative, showing that the core MDN-Pair1 interneuron circuit is re-established during metamorphosis despite profound neurite remodeling, and that this circuit coordinates forward/backward locomotion in both larvae and adults
We identified the larval Pair1 neurons based on their characteristic cell body position in the medial subesophageal zone (SEZ), dense local ipsilateral dendritic arborizations, and contralateral axons descending into the ventral nerve cord (VNC) in an extremely lateral axon tract (Carreira-Rosario et al, 2018)

Summary

Introduction

Large-scale changes in neuronal morphology and function occur during mammalian puberty (Barendse et al., 2018; Mills et al, 2016; Sisk and Zehr, 2005), as well as several neurobiological disorders including depression (Patel et al, 2019), or chronic pain (Kuner and Flor, 2017). Similar findings have been reported for the insect mushroom body, where Kenyon cells partners (projection neurons, DANs) exist at both larval and adult stages (Li et al., 2020; Marin et al, 2005) It remains unclear whether the remodeled neurons re-establish connectivity with the identical neurons in the larva and adult. We and others identified a neuron that, when activated, can trigger backward locomotion in both larvae and adults (Bidaye et al, 2014; Carreira-Rosario et al, 2018; Sen et al, 2017), despite the obvious differences in limbless and six-legged locomotion. We find that all of these questions are answered in the affirmative, showing that the core MDN-Pair interneuron circuit (a pair of synaptically-connected interneurons) is re-established during metamorphosis despite profound neurite remodeling, and that this circuit coordinates forward/backward locomotion in both larvae and adults We follow our previous work showing that MDN is remodeled during metamorphosis and persists into the adult (Carreira-Rosario et al, 2018) by asking: Is the MDN partner neuron Pair maintained in the adult? Does the adult Pair induce an inhibition in forward locomotion, similar to its role in larvae? And, are the adult Pair and MDN synaptically coupled? We find that all of these questions are answered in the affirmative, showing that the core MDN-Pair interneuron circuit (a pair of synaptically-connected interneurons) is re-established during metamorphosis despite profound neurite remodeling, and that this circuit coordinates forward/backward locomotion in both larvae and adults

Results

Discussion

Materials and Methods

10. Genotype for this and all subsequent panels