Skip to content

Research at St Andrews

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

Research output: Contribution to journalArticlepeer-review

Author(s)

Yuki Itakura, Kohsaka Hiroshi, Tomoko Ohyama, Marta Zlatic, Stefan Pulver, Akinao Nose

School/Research organisations

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.
Close

Details

Original languageEnglish
Article numbere0136660
JournalPLoS One
Volume10
Issue number9
DOIs
Publication statusPublished - 3 Sep 2015

Discover related content
Find related publications, people, projects and more using interactive charts.

View graph of relations

Related by author

  1. Inexpensive methods for live imaging of central pattern generator activity inthe Drosophila larval locomotor system

    Booth, J., Sane, V., Gather, M. C. & Pulver, S. R., 31 Dec 2020, In: Journal of Undergraduate Neuroscience Education. 19, 1, p. A124-A133

    Research output: Contribution to journalArticlepeer-review

  2. Segment-specific optogenetic stimulation in Drosophila melanogaster with linear arrays of organic light-emitting diodes

    Murawski, C., Pulver, S. R. & Gather, M. C., 7 Dec 2020, In: Nature Communications. 11, 11 p., 6248.

    Research output: Contribution to journalArticlepeer-review

  3. Narrowband organic light-emitting diodes for fluorescence microscopy and calcium imaging

    Murawski, C., Mischok, A., Booth, J. H., Kumar, J. D., Archer, E., Tropf, L. C., Keum, C., Deng, Y., Yoshida, K., Samuel, I. D. W., Schubert, M., Pulver, S. & Gather, M. C., 5 Sep 2019, In: Advanced Materials. Early View, 8 p.

    Research output: Contribution to journalArticlepeer-review

  4. New applications of organic LEDs in biophotonics

    Murawski, C., Mischok, A., Keum, C., Kumar, J. D., Pulver, S. R. & Gather, M. C., 2018, Solid-State Lighting, SSL 2018. Optical Society of American (OSA), (Optics InfoBase Conference Papers; vol. Part F117-SSL 2018).

    Research output: Chapter in Book/Report/Conference proceedingConference contribution

  5. Organic light-emitting diodes for optogenetic stimulation of Drosophila larvae

    Murawski, C., Morton, A., Samuel, I. D. W., Pulver, S. & Gather, M. C., 14 Nov 2016, Proceedings, Light, Energy and the Environment. Optical Society of American (OSA), 3 p. JW4A.9. (Fourier Transform Spectroscopy).

    Research output: Chapter in Book/Report/Conference proceedingConference contribution

Related by journal

  1. PLoS ONE (Journal)

    Joanna Louise Kershaw (Reviewer)

    18 Mar 2019

    Activity: Publication peer-review and editorial work typesPeer review of manuscripts

  2. PLoS One (Journal)

    Paula Jean Miles (Member of editorial board)

    2019

    Activity: Publication peer-review and editorial work typesPeer review of manuscripts

  3. PLoS ONE (Journal)

    Catharine Penelope Cross (Member of editorial board)

    1 Sep 2018 → …

    Activity: Publication peer-review and editorial work typesEditor of research journal

  4. PLoS ONE (Journal)

    Will Cresswell (Reviewer)

    23 May 2018

    Activity: Publication peer-review and editorial work typesPeer review of manuscripts

  5. PLoS ONE (Journal)

    Barbara Dritschel (Member of editorial board)

    May 2018 → …

    Activity: Publication peer-review and editorial work typesEditor of research journal

Related by journal

  1. Performance evaluation of survival regression models in analysing Swedish dental implant complication data with frailty

    Fagbamigbe, A. F., Karlsson, K., Derks, J. & Petzold, M., 7 Jan 2021, In: PLoS ONE. 16, 1, 16 p., e0245111.

    Research output: Contribution to journalArticlepeer-review

  2. Are in vitro and in silico approaches used appropriately for animal-based major depressive disorder research?

    Carvalho, C., Varela, S. A. M., Marques, T. A., Knight, A. & Vicente, L., 24 Jun 2020, In: PLoS ONE. 15, 6, 6 p., e0233954.

    Research output: Contribution to journalArticlepeer-review

  3. Artists on the edge of the world: an integrated approach to the study of Magdalenian engraved stone plaquettes from Jersey (Channel Islands)

    Bello, S. M., Blinkhorn, E., Needham, A., Bates, M., Duffy, S., Little, A., Pope, M., Scott, B., Shaw, A., Welch, M. D., Kinnaird, T., Millar, L., Robinson, R. & Conneller, C., 19 Aug 2020, In: PLoS ONE. 15, 8, 40 p., e0236875.

    Research output: Contribution to journalArticlepeer-review

  4. Classification and characterisation of livestock production systems in northern Tanzania

    de Glanville, W. A., Davis, A., Allan, K. J., Buza, J., Claxton, J. R., Crump, J. A., Halliday, J. E. B., Johnson, P. C. D., Kibona, T. J., Mmbaga, B. T., Swai, E. S., Uzzell, C. B., Yoder, J., Sharp, J. & Cleaveland, S., 30 Dec 2020, In: PLoS ONE. 15, 12, 25 p., e0229478.

    Research output: Contribution to journalArticlepeer-review

  5. Drivers of the opioid crisis: An appraisal of financial conflicts of interest in clinical practice guideline panels at the peak of opioid prescribing

    Spithoff, S., Leece, P., Sullivan, F., Persaud, N., Belesiotis, P. & Steiner, L., 24 Jan 2020, In: PLoS ONE. 15, 1, 15 p., e0227045.

    Research output: Contribution to journalArticlepeer-review

ID: 217975703

Top