The Frontiers in Neuroscience journal series is the 1st most cited in Neurosciences

Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Syst. Neurosci. | doi: 10.3389/fnsys.2018.00006

Neural control of startle-induced locomotion by the mushroom bodies and associated neurons in Drosophila

 Jun Sun1, An Qi Xu1, Julia Giraud1, Haiko Poppinga2, Thomas Riemensperger2, André Fiala2 and  Serge Birman1*
  • 1Brain Plasticity Unit, CNRS UMR8249, ESPCI Paris, PSL Research University, France
  • 2Johann-Friedrich-Blumenbach-Institute for Zoology and Anthropology, Georg-August-Universität Göttingen, Germany

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.

Keywords: Dopamine, Mushroom Bodies, startle-induced negative geotaxis, neural circuits, Drosophila melanogaster

Received: 14 Sep 2017; Accepted: 05 Mar 2018.

Edited by:

Irina T. Sinakevitch, Arizona State University, United States

Reviewed by:

Jean-René MARTIN, UMR9197 Institut des Neurosciences Paris Saclay (Neuro-PSI), France
Mehrab Modi, Janelia Research Campus, United States  

Copyright: © 2018 Sun, Xu, Giraud, Poppinga, Riemensperger, Fiala and Birman. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Serge Birman, ESPCI Paris, PSL Research University, Brain Plasticity Unit, CNRS UMR8249, 10 rue Vauquelin, Paris, 75005, France,