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Multiplex imaging relates quantal glutamate release to presynaptic Ca2+ homeostasis at multiple synapses in situ

Author

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  • Thomas P. Jensen

    (University College London, Queen Square)

  • Kaiyu Zheng

    (University College London, Queen Square)

  • Nicholas Cole

    (University College London, Queen Square)

  • Jonathan S. Marvin

    (Howard Hughes Medical Institute)

  • Loren L. Looger

    (Howard Hughes Medical Institute)

  • Dmitri A. Rusakov

    (University College London, Queen Square)

Abstract

Information processing by brain circuits depends on Ca2+-dependent, stochastic release of the excitatory neurotransmitter glutamate. Whilst optical glutamate sensors have enabled detection of synaptic discharges, understanding presynaptic machinery requires simultaneous readout of glutamate release and nanomolar presynaptic Ca2+ in situ. Here, we find that the fluorescence lifetime of the red-shifted Ca2+ indicator Cal-590 is Ca2+-sensitive in the nanomolar range, and employ it in combination with green glutamate sensors to relate quantal neurotransmission to presynaptic Ca2+ kinetics. Multiplexed imaging of individual and multiple synapses in identified axonal circuits reveals that glutamate release efficacy, but not its short-term plasticity, varies with time-dependent fluctuations in presynaptic resting Ca2+ or spike-evoked Ca2+ entry. Within individual presynaptic boutons, we find no nanoscopic co-localisation of evoked presynaptic Ca2+ entry with the prevalent glutamate release site, suggesting loose coupling between the two. The approach enables a better understanding of release machinery at central synapses.

Suggested Citation

  • Thomas P. Jensen & Kaiyu Zheng & Nicholas Cole & Jonathan S. Marvin & Loren L. Looger & Dmitri A. Rusakov, 2019. "Multiplex imaging relates quantal glutamate release to presynaptic Ca2+ homeostasis at multiple synapses in situ," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09216-8
    DOI: 10.1038/s41467-019-09216-8
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    Cited by:

    1. Wang, Xinyi & Zhang, Xiyun & Zheng, Muhua & Xu, Leijun & Xu, Kesheng, 2023. "Noise-induced coexisting firing patterns in hybrid-synaptic interacting networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 615(C).
    2. Philipe R. F. Mendonça & Erica Tagliatti & Helen Langley & Dimitrios Kotzadimitriou & Criseida G. Zamora-Chimal & Yulia Timofeeva & Kirill E. Volynski, 2022. "Asynchronous glutamate release is enhanced in low release efficacy synapses and dispersed across the active zone," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Ignacio Fernández-Moncada & Gianluca Lavanco & Unai B. Fundazuri & Nasrin Bollmohr & Sarah Mountadem & Tommaso Dalla Tor & Pauline Hachaguer & Francisca Julio-Kalajzic & Doriane Gisquet & Roman Serrat, 2024. "A lactate-dependent shift of glycolysis mediates synaptic and cognitive processes in male mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Céline D. Dürst & J. Simon Wiegert & Christian Schulze & Nordine Helassa & Katalin Török & Thomas G. Oertner, 2022. "Vesicular release probability sets the strength of individual Schaffer collateral synapses," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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