Determinants of synapse diversity revealed by super-resolution quantal transmission and active zone imaging

Zachary L. Newman, Dariya Bakshinskaya, Ryan Schultz, Samuel J. Kenny, Seonah Moon, Krisha Aghi, Cherise Stanley, Nadia Marnani, Rachel Li, Julia Bleier, Ke Xu and Ehud Y. Isacoff ()
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Zachary L. Newman: University of California Berkeley
Dariya Bakshinskaya: University of California Berkeley
Ryan Schultz: University of California Berkeley
Samuel J. Kenny: University of California
Seonah Moon: University of California
Krisha Aghi: University of California Berkeley
Cherise Stanley: University of California Berkeley
Nadia Marnani: University of California Berkeley
Rachel Li: University of California Berkeley
Julia Bleier: University of California Berkeley
Ke Xu: University of California Berkeley
Ehud Y. Isacoff: University of California Berkeley

Nature Communications, 2022, vol. 13, issue 1, 1-18

Abstract: Abstract Neural circuit function depends on the pattern of synaptic connections between neurons and the strength of those connections. Synaptic strength is determined by both postsynaptic sensitivity to neurotransmitter and the presynaptic probability of action potential evoked transmitter release (Pr). Whereas morphology and neurotransmitter receptor number indicate postsynaptic sensitivity, presynaptic indicators and the mechanism that sets Pr remain to be defined. To address this, we developed QuaSOR, a super-resolution method for determining Pr from quantal synaptic transmission imaging at hundreds of glutamatergic synapses at a time. We mapped the Pr onto super-resolution 3D molecular reconstructions of the presynaptic active zones (AZs) of the same synapses at the Drosophila larval neuromuscular junction (NMJ). We find that Pr varies greatly between synapses made by a single axon, quantify the contribution of key AZ proteins to Pr diversity and find that one of these, Complexin, suppresses spontaneous and evoked transmission differentially, thereby generating a spatial and quantitative mismatch between release modes. Transmission is thus regulated by the balance and nanoscale distribution of release-enhancing and suppressing presynaptic proteins to generate high signal-to-noise evoked transmission.

Date: 2022
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DOI: 10.1038/s41467-021-27815-2

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