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

Newman, Zachary L.; Bakshinskaya, Dariya; Schultz, Ryan; Kenny, Samuel J.; Moon, Seonah; Aghi, Krisha; Stanley, Cherise; Marnani, Nadia; Li, Rachel; Bleier, Julia; Xu, Ke; Isacoff, Ehud Y.

doi:10.1038/s41467-021-27815-2

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

Journal Article · 10 January 2022 · Nature Communications

DOI: https://doi.org/10.1038/s41467-021-27815-2 · OSTI ID:2470956

Newman, Zachary L. ^[1]; Bakshinskaya, Dariya ^[1]; Schultz, Ryan ^[1]; Kenny, Samuel J. ^[1]; Moon, Seonah ^[1];

^[1]; Stanley, Cherise ^[1]; Marnani, Nadia ^[1]; Li, Rachel ^[1]; Bleier, Julia ^[1];

^[2];

^[2]

University of California, Berkeley, CA (United States)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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 (P_r). Whereas morphology and neurotransmitter receptor number indicate postsynaptic sensitivity, presynaptic indicators and the mechanism that sets P_r remain to be defined. To address this, we developed QuaSOR, a super-resolution method for determining P_r from quantal synaptic transmission imaging at hundreds of glutamatergic synapses at a time. We mapped the P_r 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 P_r varies greatly between synapses made by a single axon, quantify the contribution of key AZ proteins to P_r 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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470956

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 13; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (92)

Distinct nanoscale calcium channel and synaptic vesicle topographies contribute to the diversity of synaptic function Rebola, Nelson Mendeley https://doi.org/10.17632/fjmp63fgnw.3	dataset	January 2019
Image registration by local approximation methods Goshtasby, Ardeshir Image and Vision Computing, Vol. 6, Issue 4 https://doi.org/10.1016/0262-8856(88)90016-9	journal	November 1988
Cell Type and Pathway Dependence of Synaptic AMPA Receptor Number and Variability in the Hippocampus Nusser, Zoltan; Lujan, Rafael; Laube, Gregor Neuron, Vol. 21, Issue 3 https://doi.org/10.1016/S0896-6273(00)80565-6	journal	September 1998
Inactivity Produces Increases in Neurotransmitter Release and Synapse Size Murthy, Venkatesh N.; Schikorski, Thomas; Stevens, Charles F. Neuron, Vol. 32, Issue 4 https://doi.org/10.1016/S0896-6273(01)00500-1	journal	November 2001
wishful thinking Encodes a BMP Type II Receptor that Regulates Synaptic Growth in Drosophila Aberle, Hermann; Haghighi, A. Pejmun; Fetter, Richard D. Neuron, Vol. 33, Issue 4 https://doi.org/10.1016/S0896-6273(02)00589-5	journal	February 2002
Optical Quantal Analysis Reveals a Presynaptic Component of LTP at Hippocampal Schaffer-Associational Synapses Emptage, Nigel J.; Reid, Christopher A.; Fine, Alan Neuron, Vol. 38, Issue 5 https://doi.org/10.1016/S0896-6273(03)00325-8	journal	June 2003
Multicolor Fluorescence Nanoscopy in Fixed and Living Cells by Exciting Conventional Fluorophores with a Single Wavelength Testa, Ilaria; Wurm, Christian A.; Medda, Rebecca Biophysical Journal, Vol. 99, Issue 8 https://doi.org/10.1016/j.bpj.2010.08.012	journal	October 2010
Interaction of the Complexin Accessory Helix with Synaptobrevin Regulates Spontaneous Fusion Vasin, Alexander; Volfson, Dina; Littleton, J. Troy Biophysical Journal, Vol. 111, Issue 9 https://doi.org/10.1016/j.bpj.2016.09.017	journal	November 2016
Motor neuron expression of the voltage-gated calcium channel cacophony restores locomotion defects in a Drosophila, TDP-43 loss of function model of ALS Chang, Jer-Cherng; Hazelett, Dennis J.; Stewart, Judith A. Brain Research, Vol. 1584 https://doi.org/10.1016/j.brainres.2013.11.019	journal	October 2014
A Complexin/Synaptotagmin 1 Switch Controls Fast Synaptic Vesicle Exocytosis Tang, Jiong; Maximov, Anton; Shin, Ok-Ho Cell, Vol. 126, Issue 6 https://doi.org/10.1016/j.cell.2006.08.030	journal	September 2006
Presynaptic calcium and control of vesicle fusion Schneggenburger, Ralf; Neher, Erwin Current Opinion in Neurobiology, Vol. 15, Issue 3 https://doi.org/10.1016/j.conb.2005.05.006	journal	June 2005
Creating diverse synapses from the same molecules Nusser, Zoltan Current Opinion in Neurobiology, Vol. 51 https://doi.org/10.1016/j.conb.2018.01.001	journal	August 2018
Evoked and Spontaneous Transmission Favored by Distinct Sets of Synapses Peled, Einat S.; Newman, Zachary L.; Isacoff, Ehud Y. Current Biology, Vol. 24, Issue 5 https://doi.org/10.1016/j.cub.2014.01.022	journal	March 2014
Convolution of mini distributions for fitting evoked synaptic amplitude histograms Bekkers, John M. Journal of Neuroscience Methods, Vol. 130, Issue 2 https://doi.org/10.1016/j.jneumeth.2003.09.018	journal	December 2003
Variance–mean analysis: a simple and reliable approach for investigating synaptic transmission and modulation Clements, John D. Journal of Neuroscience Methods, Vol. 130, Issue 2 https://doi.org/10.1016/j.jneumeth.2003.09.019	journal	December 2003
Examining size–strength relationships at hippocampal synapses using an ultrastructural measurement of synaptic release probability Branco, Tiago; Marra, Vincenzo; Staras, Kevin Journal of Structural Biology, Vol. 172, Issue 2 https://doi.org/10.1016/j.jsb.2009.10.014	journal	November 2010
Differential regulation of evoked and spontaneous neurotransmitter release by C-terminal modifications of complexin Buhl, Lauren K.; Jorquera, Ramon A.; Akbergenova, Yulia Molecular and Cellular Neuroscience, Vol. 52 https://doi.org/10.1016/j.mcn.2012.11.009	journal	January 2013
Molecular mechanisms of COMPLEXIN fusion clamp function in synaptic exocytosis revealed in a new Drosophila mutant Iyer, Janani; Wahlmark, Christopher J.; Kuser-Ahnert, Giselle A. Molecular and Cellular Neuroscience, Vol. 56 https://doi.org/10.1016/j.mcn.2013.06.002	journal	September 2013
Diffeomorphic demons: Efficient non-parametric image registration Vercauteren, Tom; Pennec, Xavier; Perchant, Aymeric NeuroImage, Vol. 45, Issue 1 https://doi.org/10.1016/j.neuroimage.2008.10.040	journal	March 2009
Bruchpilot, a Protein with Homology to ELKS/CAST, Is Required for Structural Integrity and Function of Synaptic Active Zones in Drosophila Wagh, Dhananjay A.; Rasse, Tobias M.; Asan, Esther Neuron, Vol. 49, Issue 6 https://doi.org/10.1016/j.neuron.2006.02.008	journal	March 2006
State-Dependent Mechanisms of LTP Expression Revealed by Optical Quantal Analysis Ward, Bonnie; McGuinness, Lindsay; Akerman, Colin J. Neuron, Vol. 52, Issue 4 https://doi.org/10.1016/j.neuron.2006.10.007	journal	November 2006
Expression of Long-Term Plasticity at Individual Synapses in Hippocampus Is Graded, Bidirectional, and Mainly Presynaptic: Optical Quantal Analysis Enoki, Ryosuke; Hu, Yi-ling; Hamilton, David Neuron, Vol. 62, Issue 2 https://doi.org/10.1016/j.neuron.2009.02.026	journal	April 2009
Tilting the Balance between Facilitatory and Inhibitory Functions of Mammalian and Drosophila Complexins Orchestrates Synaptic Vesicle Exocytosis Xue, Mingshan; Lin, Yong Qi; Pan, Hongling Neuron, Vol. 64, Issue 3 https://doi.org/10.1016/j.neuron.2009.09.043	journal	November 2009
The Presynaptic Active Zone Südhof, Thomas C. Neuron, Vol. 75, Issue 1 https://doi.org/10.1016/j.neuron.2012.06.012	journal	July 2012
Phosphorylation of Complexin by PKA Regulates Activity-Dependent Spontaneous Neurotransmitter Release and Structural Synaptic Plasticity Cho, Richard W.; Buhl, Lauren K.; Volfson, Dina Neuron, Vol. 88, Issue 4 https://doi.org/10.1016/j.neuron.2015.10.011	journal	November 2015
Input-Specific Plasticity and Homeostasis at the Drosophila Larval Neuromuscular Junction Newman, Zachary L.; Hoagland, Adam; Aghi, Krishan Neuron, Vol. 93, Issue 6 https://doi.org/10.1016/j.neuron.2017.02.028	journal	March 2017
Spatiotemporal Regulation of Synaptic Vesicle Fusion Sites in Central Synapses Maschi, Dario; Klyachko, Vitaly A. Neuron, Vol. 94, Issue 1 https://doi.org/10.1016/j.neuron.2017.03.006	journal	April 2017
Stable Positioning of Unc13 Restricts Synaptic Vesicle Fusion to Defined Release Sites to Promote Synchronous Neurotransmission Reddy-Alla, Suneel; Böhme, Mathias A.; Reynolds, Eric Neuron, Vol. 95, Issue 6 https://doi.org/10.1016/j.neuron.2017.08.016	journal	September 2017
Distinct Nanoscale Calcium Channel and Synaptic Vesicle Topographies Contribute to the Diversity of Synaptic Function Rebola, Nelson; Reva, Maria; Kirizs, Tekla Neuron, Vol. 104, Issue 4 https://doi.org/10.1016/j.neuron.2019.08.014	journal	November 2019
Imaging Neurotransmitter and Neuromodulator Dynamics In Vivo with Genetically Encoded Indicators Sabatini, Bernardo L.; Tian, Lin Neuron, Vol. 108, Issue 1 https://doi.org/10.1016/j.neuron.2020.09.036	journal	October 2020
Quantitative Data Analysis in Single-Molecule Localization Microscopy Wu, Yu-Le; Tschanz, Aline; Krupnik, Leonard Trends in Cell Biology, Vol. 30, Issue 11 https://doi.org/10.1016/j.tcb.2020.07.005	journal	November 2020
Nanoscale Organization of Vesicle Release at Central Synapses Gramlich, Michael W.; Klyachko, Vitaly A. Trends in Neurosciences, Vol. 42, Issue 6 https://doi.org/10.1016/j.tins.2019.03.001	journal	June 2019
Multicolor Far-Field Fluorescence Nanoscopy through Isolated Detection of Distinct Molecular Species Bossi, Mariano; Fölling, Jonas; Belov, Vladimir N. Nano Letters, Vol. 8, Issue 8 https://doi.org/10.1021/nl801471d	journal	August 2008
Intracellular calcium dependence of transmitter release rates at a fast central synapse Schneggenburger, Ralf; Neher, Erwin Nature, Vol. 406, Issue 6798 https://doi.org/10.1038/35022702	journal	August 2000
Calcium influx and transmitter release in a fast CNS synapse Borst, J. G. G.; Sakmann, B. Nature, Vol. 383, Issue 6599 https://doi.org/10.1038/383431a0	journal	October 1996
A trans-synaptic nanocolumn aligns neurotransmitter release to receptors Tang, Ai-Hui; Chen, Haiwen; Li, Tuo P. Nature, Vol. 536, Issue 7615 https://doi.org/10.1038/nature19058	journal	July 2016
Quantitative super-resolution imaging of Bruchpilot distinguishes active zone states Ehmann, Nadine; van de Linde, Sebastian; Alon, Amit Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5650	journal	August 2014
Graphene-enabled electron microscopy and correlated super-resolution microscopy of wet cells Wojcik, Michal; Hauser, Margaret; Li, Wan Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8384	journal	June 2015
Fluorophore localization algorithms for super-resolution microscopy Small, Alex; Stahlheber, Shane Nature Methods, Vol. 11, Issue 3 https://doi.org/10.1038/nmeth.2844	journal	February 2014
Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) Rust, Michael J.; Bates, Mark; Zhuang, Xiaowei Nature Methods, Vol. 3, Issue 10 https://doi.org/10.1038/nmeth929	journal	August 2006
Optical quantal analysis of synaptic transmission in wild-type and rab3-mutant Drosophila motor axons Peled, Einat S.; Isacoff, Ehud Y. Nature Neuroscience, Vol. 14, Issue 4 https://doi.org/10.1038/nn.2767	journal	March 2011
Release probability of hippocampal glutamatergic terminals scales with the size of the active zone Holderith, Noemi; Lorincz, Andrea; Katona, Gergely Nature Neuroscience, Vol. 15, Issue 7 https://doi.org/10.1038/nn.3137	journal	June 2012
A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth Huntwork, Sarah; Littleton, J. Troy Nature Neuroscience, Vol. 10, Issue 10 https://doi.org/10.1038/nn1980	journal	September 2007
Facilitation at single synapses probed with optical quantal analysis Oertner, Thomas G.; Sabatini, Bernardo L.; Nimchinsky, Esther A. Nature Neuroscience, Vol. 5, Issue 7 https://doi.org/10.1038/nn867	journal	June 2002
Should I stop or should I go? The role of complexin in neurotransmitter release Trimbuch, Thorsten; Rosenmund, Christian Nature Reviews Neuroscience, Vol. 17, Issue 2 https://doi.org/10.1038/nrn.2015.16	journal	January 2016
Experience-dependent structural synaptic plasticity in the mammalian brain Holtmaat, Anthony; Svoboda, Karel Nature Reviews Neuroscience, Vol. 10, Issue 9 https://doi.org/10.1038/nrn2699	journal	September 2009
Deep molecular diversity of mammalian synapses: why it matters and how to measure it O'Rourke, Nancy A.; Weiler, Nicholas C.; Micheva, Kristina D. Nature Reviews Neuroscience, Vol. 13, Issue 6 https://doi.org/10.1038/nrn3170	journal	May 2012
Hemifusion arrest by complexin is relieved by Ca2+–synaptotagmin I Schaub, Johanna R.; Lu, Xiaobing; Doneske, Blair Nature Structural & Molecular Biology, Vol. 13, Issue 8 https://doi.org/10.1038/nsmb1124	journal	July 2006
Underpinning heterogeneity in synaptic transmission by presynaptic ensembles of distinct morphological modules Fekete, Adam; Nakamura, Yukihiro; Yang, Yi-Mei Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08452-2	journal	February 2019
Super-resolution microscopy demystified Schermelleh, Lothar; Ferrand, Alexia; Huser, Thomas Nature Cell Biology, Vol. 21, Issue 1 https://doi.org/10.1038/s41556-018-0251-8	journal	January 2019
The control of release probability at nerve terminals Dittman, Jeremy S.; Ryan, Timothy A. Nature Reviews Neuroscience, Vol. 20, Issue 3 https://doi.org/10.1038/s41583-018-0111-3	journal	January 2019
Neuronal plasticity affects correlation between the size of dendritic spine and its postsynaptic density Borczyk, Malgorzata; Śliwińska, Małgorzata Alicja; Caly, Anna Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-38412-7	journal	February 2019
Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release Matz, Jacob; Gilyan, Andrew; Kolar, Annette Proceedings of the National Academy of Sciences, Vol. 107, Issue 19 https://doi.org/10.1073/pnas.0906087107	journal	April 2010
Functional reconstitution of Drosophila melanogaster NMJ glutamate receptors Han, Tae Hee; Dharkar, Poorva; Mayer, Mark L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1500458112	journal	April 2015
Three-dimensional imaging of Drosophila motor synapses reveals ultrastructural organizational patterns Zhan, Hong; Bruckner, Joseph; Zhang, Ziheng Journal of Neurogenetics, Vol. 30, Issue 3-4 https://doi.org/10.1080/01677063.2016.1253693	journal	October 2016
Maturation of active zone assembly by Drosophila Bruchpilot Fouquet, Wernher; Owald, David; Wichmann, Carolin Journal of Cell Biology, Vol. 186, Issue 1 https://doi.org/10.1083/jcb.200812150	journal	July 2009
Fife organizes synaptic vesicles and calcium channels for high-probability neurotransmitter release Bruckner, Joseph J.; Zhan, Hong; Gratz, Scott J. Journal of Cell Biology, Vol. 216, Issue 1 https://doi.org/10.1083/jcb.201601098	journal	December 2016
COPII-coated membranes function as transport carriers of intracellular procollagen I Gorur, Amita; Yuan, Lin; Kenny, Samuel J. Journal of Cell Biology, Vol. 216, Issue 6 https://doi.org/10.1083/jcb.201702135	journal	April 2017
Complexin cooperates with Bruchpilot to tether synaptic vesicles to the active zone cytomatrix Scholz, Nicole; Ehmann, Nadine; Sachidanandan, Divya Journal of Cell Biology, Vol. 218, Issue 3 https://doi.org/10.1083/jcb.201806155	journal	February 2019
Resolution improvement by 3D particle averaging in localization microscopy Broeken, Jordi; Johnson, Hannah; Lidke, Diane S. Methods and Applications in Fluorescence, Vol. 3, Issue 1 https://doi.org/10.1088/2050-6120/3/1/014003	journal	January 2015
Globally optimal stitching of tiled 3D microscopic image acquisitions Preibisch, S.; Saalfeld, S.; Tomancak, P. Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp184	journal	April 2009
Rings, circles, and null-models for point pattern analysis in ecology Wiegand, Thorsten; A. Moloney, Kirk Oikos, Vol. 104, Issue 2 https://doi.org/10.1111/j.0030-1299.2004.12497.x	journal	February 2004
Co‐operative action of calcium ions in transmitter release at the neuromuscular junction Dodge, F. A.; Rahamimoff, R. The Journal of Physiology, Vol. 193, Issue 2 https://doi.org/10.1113/jphysiol.1967.sp008367	journal	November 1967
Properties of the larval neuromuscular junction in Drosophila melanogaster. Jan, L. Y.; Jan, Y. N. The Journal of Physiology, Vol. 262, Issue 1 https://doi.org/10.1113/jphysiol.1976.sp011592	journal	October 1976
Target Cell-Dependent Normalization of Transmitter Release at Neocortical Synapses Koester, H. J. Science, Vol. 308, Issue 5723 https://doi.org/10.1126/science.1100815	journal	May 2005
Bruchpilot Promotes Active Zone Assembly, Ca2+ Channel Clustering, and Vesicle Release Kittel, R. J. Science, Vol. 312, Issue 5776 https://doi.org/10.1126/science.1126308	journal	May 2006
A Clamping Mechanism Involved in SNARE-Dependent Exocytosis Giraudo, C. G. Science, Vol. 313, Issue 5787 https://doi.org/10.1126/science.1129450	journal	August 2006
Three-Dimensional Super-Resolution Imaging by Stochastic Optical Reconstruction Microscopy Huang, B.; Wang, W.; Bates, M. Science, Vol. 319, Issue 5864 https://doi.org/10.1126/science.1153529	journal	February 2008
RIM-Binding Protein, a Central Part of the Active Zone, Is Essential for Neurotransmitter Release Liu, Karen S. Y.; Siebert, Matthias; Mertel, Sara Science, Vol. 334, Issue 6062 https://doi.org/10.1126/science.1212991	journal	December 2011
Nuclear Pore Scaffold Structure Analyzed by Super-Resolution Microscopy and Particle Averaging Szymborska, A.; de Marco, A.; Daigle, N. Science, Vol. 341, Issue 6146 https://doi.org/10.1126/science.1240672	journal	July 2013
Single-vesicle imaging reveals different transport mechanisms between glutamatergic and GABAergic vesicles Farsi, Zohreh; Preobraschenski, Julia; van den Bogaart, Geert Science, Vol. 351, Issue 6276 https://doi.org/10.1126/science.aad8142	journal	February 2016
The Synaptic Vesicle Release Machinery Rizo, Josep; Xu, Junjie Annual Review of Biophysics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-biophys-060414-034057	journal	June 2015
Molecular Mechanisms of Fast Neurotransmitter Release Brunger, Axel T.; Choi, Ucheor B.; Lai, Ying Annual Review of Biophysics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-biophys-070816-034117	journal	May 2018
Efficient subpixel image registration algorithms Guizar-Sicairos, Manuel; Thurman, Samuel T.; Fienup, James R. Optics Letters, Vol. 33, Issue 2 https://doi.org/10.1364/OL.33.000156	journal	January 2008
Nitric oxide-mediated posttranslational modifications control neurotransmitter release by modulating complexin farnesylation and enhancing its clamping ability Robinson, Susan W.; Bourgognon, Julie-Myrtille; Spiers, Jereme G. PLOS Biology, Vol. 16, Issue 4 https://doi.org/10.1371/journal.pbio.2003611	journal	April 2018
Activity-Dependent Global Downscaling of Evoked Neurotransmitter Release across Glutamatergic Inputs inDrosophila Karunanithi, Shanker; Lin, Yong Qi; Odierna, G. Lorenzo The Journal of Neuroscience, Vol. 40, Issue 42 https://doi.org/10.1523/JNEUROSCI.0349-20.2020	journal	September 2020
Quantitative Ultrastructural Analysis of Hippocampal Excitatory Synapses Schikorski, Thomas; Stevens, Charles F. The Journal of Neuroscience, Vol. 17, Issue 15 https://doi.org/10.1523/JNEUROSCI.17-15-05858.1997	journal	August 1997
Mechanisms of Calcium Influx into Hippocampal Spines: Heterogeneity among Spines, Coincidence Detection by NMDA Receptors, and Optical Quantal Analysis Yuste, Rafael; Majewska, Ania; Cash, Sydney S. The Journal of Neuroscience, Vol. 19, Issue 6 https://doi.org/10.1523/JNEUROSCI.19-06-01976.1999	journal	March 1999
Spontaneous and Evoked Glutamate Release Activates Two Populations of NMDA Receptors with Limited Overlap Atasoy, Deniz; Ertunc, Mert; Moulder, Krista L. The Journal of Neuroscience, Vol. 28, Issue 40 https://doi.org/10.1523/JNEUROSCI.2432-08.2008	journal	October 2008
Naked Dense Bodies Provoke Depression Hallermann, Stefan; Kittel, Robert J.; Wichmann, Carolin The Journal of Neuroscience, Vol. 30, Issue 43 https://doi.org/10.1523/JNEUROSCI.2495-10.2010	journal	October 2010
Complexin Controls Spontaneous and Evoked Neurotransmitter Release by Regulating the Timing and Properties of Synaptotagmin Activity Jorquera, R. A.; Huntwork-Rodriguez, S.; Akbergenova, Y. Journal of Neuroscience, Vol. 32, Issue 50 https://doi.org/10.1523/JNEUROSCI.3212-12.2012	journal	December 2012
Spontaneous and Evoked Release Are Independently Regulated at Individual Active Zones Melom, Jan E.; Akbergenova, Yulia; Gavornik, Jeffrey P. The Journal of Neuroscience, Vol. 33, Issue 44 https://doi.org/10.1523/JNEUROSCI.3334-13.2013	journal	October 2013
Active Zone Localization of Presynaptic Calcium Channels Encoded by thecacophonyLocus ofDrosophila Kawasaki, Fumiko; Zou, Beiyan; Xu, Xia The Journal of Neuroscience, Vol. 24, Issue 1 https://doi.org/10.1523/JNEUROSCI.3553-03.2004	journal	January 2004
Optical Quantal Analysis Indicates That Long-Term Potentiation at Single Hippocampal Mossy Fiber Synapses Is Expressed through Increased Release Probability, Recruitment of New Release Sites, and Activation of Silent Synapses Reid, Christopher A.; Dixon, Don B.; Takahashi, Michiko The Journal of Neuroscience, Vol. 24, Issue 14 https://doi.org/10.1523/JNEUROSCI.3567-03.2004	journal	April 2004
Number and Density of AMPA Receptors in Single Synapses in Immature Cerebellum Tanaka, Jun-ichi; Matsuzaki, Masanori; Tarusawa, Etsuko The Journal of Neuroscience, Vol. 25, Issue 4 https://doi.org/10.1523/JNEUROSCI.4256-04.2005	journal	January 2005
Presynaptic Mitochondria in Functionally Different Motor Neurons Exhibit Similar Affinities for Ca²⁺But Exert Little Influence as Ca²⁺Buffers at Nerve Firing RatesIn Situ Chouhan, Amit K.; Zhang, Jinhui; Zinsmaier, Konrad E. The Journal of Neuroscience, Vol. 30, Issue 5 https://doi.org/10.1523/JNEUROSCI.4701-09.2010	journal	February 2010
Distinct nanoscale calcium channel and synaptic vesicle topographies contribute to the diversity of synaptic function Rebola, Nelson Mendeley https://doi.org/10.17632/fjmp63fgnw.3	dataset	January 2019
Optical mapping of release properties in synapses Frontiers in Neural Circuits https://doi.org/10.3389/fncir.2010.00018	journal	January 2010
Optical Quantal Analysis Using Ca2+ Indicators: A Robust Method for Assessing Transmitter Release Probability at Excitatory Synapses by Imaging Single Glutamate Release Events Padamsey, Zahid; Tong, Rudi; Emptage, Nigel Frontiers in Synaptic Neuroscience, Vol. 11 https://doi.org/10.3389/fnsyn.2019.00005	journal	March 2019
Optical Quantal Analysis MacDougall, Matthew J.; Fine, Alan Frontiers in Synaptic Neuroscience, Vol. 11 https://doi.org/10.3389/fnsyn.2019.00008	journal	March 2019
Source Data File: Determinants of synapse diversity revealed by super-resolution quantal transmission and active zone imaging Newman, Zachary figshare https://doi.org/10.6084/m9.figshare.17041718.v1	dataset	January 2021
Characterization of developmental and molecular factors underlying release heterogeneity at Drosophila synapses Akbergenova, Yulia; Cunningham, Karen L.; Zhang, Yao V. eLife, Vol. 7 https://doi.org/10.7554/eLife.38268	journal	July 2018

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

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