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Identification of inhibitory premotor interneurons activated at a late phase in a motor cycle during Drosophila larval locomotion

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journal.pone.0136660.pdf (12.48Mb)
Date
03/09/2015
Author
Itakura, Yuki
Hiroshi, Kohsaka
Ohyama, Tomoko
Zlatic, Marta
Pulver, Stefan
Nose, Akinao
Keywords
RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
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Abstract
Rhythmic motor patterns underlying many types of locomotion are thought to be produced by central pattern generators (CPGs). Our knowledge of how CPG networks generate motor patterns in complex nervous systems remains incomplete, despite decades of work in a variety of model organisms. Substrate borne locomotion in Drosophila larvae is driven by waves of muscular contraction that propagate through multiple body segments. We use the motor circuitry underlying crawling in larval Drosophila as a model to try to understand how segmentally coordinated rhythmic motor patterns are generated. Whereas muscles, motoneurons and sensory neurons have been well investigated in this system, far less is known about the identities and function of interneurons. Our recent study identified a class of glutamatergic premotor interneurons, PMSIs (period-positive median segmental interneurons), that regulate the speed of locomotion. Here, we report on the identification of a distinct class of glutamatergic premotor interneurons called Glutamatergic Ventro-Lateral Interneurons (GVLIs). We used calcium imaging to search for interneurons that show rhythmic activity and identified GVLIs as interneurons showing wave-like activity during peristalsis. Paired GVLIs were present in each abdominal segment A1-A7 and locally extended an axon towards a dorsal neuropile region, where they formed GRASP-positive putative synaptic contacts with motoneurons. The interneurons expressed vesicular glutamate transporter (vGluT) and thus likely secrete glutamate, a neurotransmitter known to inhibit motoneurons. These anatomical results suggest that GVLIs are premotor interneurons that locally inhibit motoneurons in the same segment. Consistent with this, optogenetic activation of GVLIs with the red-shifted channelrhodopsin, CsChrimson ceased ongoing peristalsis in crawling larvae. Simultaneous calcium imaging of the activity of GVLIs and motoneurons showed that GVLIs' wave-like activity lagged behind that of motoneurons by several segments. Thus, GVLIs are activated when the front of a forward motor wave reaches the second or third anterior segment. We propose that GVLIs are part of the feedback inhibition system that terminates motor activity once the front of the motor wave proceeds to anterior segments.
Citation
Itakura , Y , Hiroshi , K , Ohyama , T , Zlatic , M , Pulver , S & Nose , A 2015 , ' Identification of inhibitory premotor interneurons activated at a late phase in a motor cycle during Drosophila larval locomotion ' , PLoS One , vol. 10 , no. 9 , e0136660 . https://doi.org/10.1371/journal.pone.0136660
Publication
PLoS One
Status
Peer reviewed
DOI
https://doi.org/10.1371/journal.pone.0136660
ISSN
1932-6203
Type
Journal article
Rights
© 2015 Itakura et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
Description
This work was supported by a MEXT/JSPS KAKENHI Grant Numbers, 22115002 (to A.N.) and 221S0003 (to A.N. and Y.I.), and 15H04255 (to A.N.). The work was also supported by Janelia Research Campus (Howard Hughes Medical Institute).
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  • University of St Andrews Research
URL
http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0136660#sec021
URI
http://hdl.handle.net/10023/7515

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