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

Adam Fekete, Yukihiro Nakamura, Yi-Mei Yang, Stefan Herlitze, Melanie D. Mark, David A. DiGregorio and Lu-Yang Wang ()
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Adam Fekete: The Hospital for Sick Children
Yukihiro Nakamura: Jikei University School of Medicine, Nishishinbashi, Minato-ku
Yi-Mei Yang: The Hospital for Sick Children
Stefan Herlitze: Ruhr-University Bochum
Melanie D. Mark: Ruhr-University Bochum
David A. DiGregorio: Unit of Dynamic Neuronal Imaging, Institut Pasteur
Lu-Yang Wang: The Hospital for Sick Children

Nature Communications, 2019, vol. 10, issue 1, 1-16

Abstract: 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.

Date: 2019
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DOI: 10.1038/s41467-019-08452-2

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