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Underpinning heterogeneity in synaptic transmission by presynaptic ensembles of distinct morphological modules

Author

Listed:
  • Adam Fekete

    (The Hospital for Sick Children
    University of Toronto)

  • Yukihiro Nakamura

    (Jikei University School of Medicine, Nishishinbashi, Minato-ku)

  • Yi-Mei Yang

    (The Hospital for Sick Children
    University of Toronto
    University of Minnesota Medical School)

  • Stefan Herlitze

    (Ruhr-University Bochum)

  • Melanie D. Mark

    (Ruhr-University Bochum)

  • David A. DiGregorio

    (Unit of Dynamic Neuronal Imaging, Institut Pasteur
    Centre National de la Recherche Scientifique (CNRS), UMR 3571, Genes, Synapses and Cognition, Institut Pasteur)

  • Lu-Yang Wang

    (The Hospital for Sick Children
    University of Toronto)

Abstract

Synaptic heterogeneity is widely observed but its underpinnings remain elusive. We addressed this issue using mature calyx of Held synapses whose numbers of bouton-like swellings on stalks of the nerve terminals inversely correlate with release probability (Pr). We examined presynaptic Ca2+ currents and transients, topology of fluorescently tagged knock-in Ca2+ channels, and Ca2+ channel-synaptic vesicle (SV) coupling distance using Ca2+ chelator and inhibitor of septin cytomatrix in morphologically diverse synapses. We found that larger clusters of Ca2+ channels with tighter coupling distance to SVs elevate Pr in stalks, while smaller clusters with looser coupling distance lower Pr in swellings. Septin is a molecular determinant of the differences in coupling distance. Supported by numerical simulations, we propose that varying the ensemble of two morphological modules containing distinct Ca2+ channel-SV topographies diversifies Pr in the terminal, thereby establishing a morpho-functional continuum that expands the coding capacity within a single synapse population.

Suggested Citation

  • Adam Fekete & Yukihiro Nakamura & Yi-Mei Yang & Stefan Herlitze & Melanie D. Mark & David A. DiGregorio & Lu-Yang Wang, 2019. "Underpinning heterogeneity in synaptic transmission by presynaptic ensembles of distinct morphological modules," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-08452-2
    DOI: 10.1038/s41467-019-08452-2
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