Neural Control of Startle-Induced Locomotion by the Mushroom Bodies and Associated Neurons in Drosophila.

Jun Sun,An Qi Xu,André Fiala,Thomas Riemensperger,Haiko Poppinga,Serge Birman,Julia Giraud

doi:10.3389/fnsys.2018.00006

Abstract

Startle-induced locomotion is commonly used in Drosophila research to monitor locomotor reactivity and its progressive decline with age or under various neuropathological conditions. A widely used paradigm is startle-induced negative geotaxis (SING), in which flies entrapped in a narrow column react to a gentle mechanical shock by climbing rapidly upwards. Here we combined in vivo manipulation of neuronal activity and splitGFP reconstitution across cells to search for brain neurons and putative circuits that regulate this behavior. We show that the activity of specific clusters of dopaminergic neurons (DANs) afferent to the mushroom bodies (MBs) modulates SING, and that DAN-mediated SING regulation requires expression of the DA receptor Dop1R1/Dumb, but not Dop1R2/Damb, in intrinsic MB Kenyon cells (KCs). We confirmed our previous observation that activating the MB α'β', but not αβ, KCs decreased the SING response, and we identified further MB neurons implicated in SING control, including KCs of the γ lobe and two subtypes of MB output neurons (MBONs). We also observed that co-activating the αβ KCs antagonizes α'β' and γ KC-mediated SING modulation, suggesting the existence of subtle regulation mechanisms between the different MB lobes in locomotion control. Overall, this study contributes to an emerging picture of the brain circuits modulating locomotor reactivity in Drosophila that appear both to overlap and differ from those underlying associative learning and memory, sleep/wake state and stress-induced hyperactivity.

Highlights

The identification of neural circuits that modulate innate or reflex behaviors is essential to better understand how the brain functions and adapts to a changing environment (LeBeau et al, 2005; Dickinson, 2006; Marder, 2012; Su and Wang, 2014)
We have recently reported that the degeneration of dopaminergic neuron (DAN) of either the protocerebral anterior medial (PAM) or protocerebral posterior lateral 1 (PPL1) clusters afferent to the mushroom body (MB) was associated with an accelerated decline of startle-induced negative geotaxis (SING) performance in aging flies (Riemensperger et al, 2013; Vaccaro et al, 2017)
After a 10-min incubation, these tyrosine hydroxylase (TH)>shits1 flies showed no difference in SING performance between the permissive (23◦C) and restrictive (32◦C) temperatures, indicating that TH-Gal4targeted DANs are not required for the execution of this locomotor response (Figure 1A)

Summary

Introduction

The identification of neural circuits that modulate innate or reflex behaviors is essential to better understand how the brain functions and adapts to a changing environment (LeBeau et al, 2005; Dickinson, 2006; Marder, 2012; Su and Wang, 2014). Neuromodulation of Drosophila Startle-Induced Locomotion organism, spontaneous locomotor activity and locomotor reactivity have been described as two separate behavioral systems that are regulated differently (Connolly, 1967; Meehan and Wilson, 1987; O’Dell and Burnet, 1988; Martin et al, 1999a). Startle-induced reactivity has long been used in Drosophila to monitor various behavioral performances, such as phototaxis (Benzer, 1967) or negative geotaxis (Miquel et al, 1972). A widely used paradigm relies on the fast climbing reaction initiated by a gentle mechanical shock of flies entrapped in a vial or a narrow column, an innate reflex called startle-induced negative geotaxis (SING). It is of particular interest to identify precise neural components underlying the modulation of startle-induced locomotion, in Drosophila as in other species (Hale et al, 2016)

Methods

Results

Conclusion