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Glutamate spillover in C. elegans triggers repetitive behavior through presynaptic activation of MGL-2/mGluR5

Author

Listed:
  • Menachem Katz

    (The Rockefeller University)

  • Francis Corson

    (Université Paris Diderot)

  • Wolfgang Keil

    (The Rockefeller University
    The Rockefeller University)

  • Anupriya Singhal

    (The Rockefeller University)

  • Andrea Bae

    (The Rockefeller University)

  • Yun Lu

    (The Rockefeller University)

  • Yupu Liang

    (The Rockefeller University)

  • Shai Shaham

    (The Rockefeller University)

Abstract

Glutamate is a major excitatory neurotransmitter, and impaired glutamate clearance following synaptic release promotes spillover, inducing extra-synaptic signaling. The effects of glutamate spillover on animal behavior and its neural correlates are poorly understood. We developed a glutamate spillover model in Caenorhabditis elegans by inactivating the conserved glial glutamate transporter GLT-1. GLT-1 loss drives aberrant repetitive locomotory reversal behavior through uncontrolled oscillatory release of glutamate onto AVA, a major interneuron governing reversals. Repetitive glutamate release and reversal behavior require the glutamate receptor MGL-2/mGluR5, expressed in RIM and other interneurons presynaptic to AVA. mgl-2 loss blocks oscillations and repetitive behavior; while RIM activation is sufficient to induce repetitive reversals in glt-1 mutants. Repetitive AVA firing and reversals require EGL-30/Gαq, an mGluR5 effector. Our studies reveal that cyclic autocrine presynaptic activation drives repetitive reversals following glutamate spillover. That mammalian GLT1 and mGluR5 are implicated in pathological motor repetition suggests a common mechanism controlling repetitive behaviors.

Suggested Citation

  • Menachem Katz & Francis Corson & Wolfgang Keil & Anupriya Singhal & Andrea Bae & Yun Lu & Yupu Liang & Shai Shaham, 2019. "Glutamate spillover in C. elegans triggers repetitive behavior through presynaptic activation of MGL-2/mGluR5," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09581-4
    DOI: 10.1038/s41467-019-09581-4
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    Cited by:

    1. Jung-Hwan Choi & Lauren Bayer Horowitz & Niels Ringstad, 2021. "Opponent vesicular transporters regulate the strength of glutamatergic neurotransmission in a C. elegans sensory circuit," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Francesca Coraggio & Mahak Bhushan & Spyridon Roumeliotis & Francesca Caroti & Carlo Bevilacqua & Robert Prevedel & Georgia Rapti, 2024. "Age-progressive interplay of HSP-proteostasis, ECM-cell junctions and biomechanics ensures C. elegans astroglial architecture," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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