IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0013514.html
   My bibliography  Save this article

Synapse Clusters Are Preferentially Formed by Synapses with Large Recycling Pool Sizes

Author

Listed:
  • Oliver Welzel
  • Carsten H Tischbirek
  • Jasmin Jung
  • Eva M Kohler
  • Alexei Svetlitchny
  • Andreas W Henkel
  • Johannes Kornhuber
  • Teja W Groemer

Abstract

Synapses are distributed heterogeneously in neural networks. The relationship between the spatial arrangement of synapses and an individual synapse's structural and functional features remains to be elucidated. Here, we examined the influence of the number of adjacent synapses on individual synaptic recycling pool sizes. When measuring the discharge of the styryl dye FM1–43 from electrically stimulated synapses in rat hippocampal tissue cultures, a strong positive correlation between the number of neighbouring synapses and recycling vesicle pool sizes was observed. Accordingly, vesicle-rich synapses were found to preferentially reside next to neighbours with large recycling pool sizes. Although these synapses with large recycling pool sizes were rare, they were densely arranged and thus exhibited a high amount of release per volume. To consolidate these findings, functional terminals were marked by live-cell antibody staining with anti-synaptotagmin-1-cypHer or overexpression of synaptopHluorin. Analysis of synapse distributions in these systems confirmed the results obtained with FM 1–43. Our findings support the idea that clustering of synapses with large recycling pool sizes is a distinct developmental feature of newly formed neural networks and may contribute to functional plasticity.

Suggested Citation

  • Oliver Welzel & Carsten H Tischbirek & Jasmin Jung & Eva M Kohler & Alexei Svetlitchny & Andreas W Henkel & Johannes Kornhuber & Teja W Groemer, 2010. "Synapse Clusters Are Preferentially Formed by Synapses with Large Recycling Pool Sizes," PLOS ONE, Public Library of Science, vol. 5(10), pages 1-9, October.
    • Handle: RePEc:plo:pone00:0013514
    DOI: 10.1371/journal.pone.0013514
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0013514
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0013514&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0013514?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Gina G. Turrigiano & Kenneth R. Leslie & Niraj S. Desai & Lana C. Rutherford & Sacha B. Nelson, 1998. "Activity-dependent scaling of quantal amplitude in neocortical neurons," Nature, Nature, vol. 391(6670), pages 892-896, February.
    2. Gero Miesenböck & Dino A. De Angelis & James E. Rothman, 1998. "Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins," Nature, Nature, vol. 394(6689), pages 192-195, July.
    3. D. B. Chklovskii & B. W. Mel & K. Svoboda, 2004. "Cortical rewiring and information storage," Nature, Nature, vol. 431(7010), pages 782-788, October.
    4. Timothy A. Ryan & Harald Reuter & Stephen J Smith, 1997. "Optical detection of a quantal presynaptic membrane turnover," Nature, Nature, vol. 388(6641), pages 478-482, July.
    5. Venkatesh N. Murthy & Charles F. Stevens, 1998. "Synaptic vesicles retain their identity through the endocytic cycle," Nature, Nature, vol. 392(6675), pages 497-501, April.
    6. A. M. Aravanis & J. L. Pyle & R. W. Tsien, 2003. "Single synaptic vesicles fusing transiently and successively without loss of identity," Nature, Nature, vol. 423(6940), pages 643-647, June.
    7. Graeme W. Davis & Corey S. Goodman, 1998. "Synapse-specific control of synaptic efficacy at the terminals of a single neuron," Nature, Nature, vol. 392(6671), pages 82-86, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Tiziano D’Albis & Richard Kempter, 2017. "A single-cell spiking model for the origin of grid-cell patterns," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-41, October.
    2. Mable Lam & Koji Takeo & Rafael G. Almeida & Madeline H. Cooper & Kathryn Wu & Manasi Iyer & Husniye Kantarci & J. Bradley Zuchero, 2022. "CNS myelination requires VAMP2/3-mediated membrane expansion in oligodendrocytes," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    3. Katerina Karkali & Samuel W. Vernon & Richard A. Baines & George Panayotou & Enrique Martín-Blanco, 2023. "Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Matteo Saponati & Martin Vinck, 2023. "Sequence anticipation and spike-timing-dependent plasticity emerge from a predictive learning rule," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Niranjan Chakravarthy & Shivkumar Sabesan & Kostas Tsakalis & Leon Iasemidis, 2009. "Controlling epileptic seizures in a neural mass model," Journal of Combinatorial Optimization, Springer, vol. 17(1), pages 98-116, January.
    6. Damien M O’Halloran, 2020. "Simulation model of CA1 pyramidal neurons reveal opposing roles for the Na+/Ca2+ exchange current and Ca2+-activated K+ current during spike-timing dependent synaptic plasticity," PLOS ONE, Public Library of Science, vol. 15(3), pages 1-12, March.
    7. Fausto-Sterling, Anne & Coll, Cynthia Garcia & Lamarre, Meaghan, 2012. "Sexing the baby: Part 2 applying dynamic systems theory to the emergences of sex-related differences in infants and toddlers," Social Science & Medicine, Elsevier, vol. 74(11), pages 1693-1702.
    8. Spencer L Smith & Joshua T Trachtenberg, 2010. "The Refinement of Ipsilateral Eye Retinotopic Maps Is Increased by Removing the Dominant Contralateral Eye in Adult Mice," PLOS ONE, Public Library of Science, vol. 5(3), pages 1-6, March.
    9. Sacha Jennifer van Albada & Moritz Helias & Markus Diesmann, 2015. "Scalability of Asynchronous Networks Is Limited by One-to-One Mapping between Effective Connectivity and Correlations," PLOS Computational Biology, Public Library of Science, vol. 11(9), pages 1-37, September.
    10. Dean J. Kareemo & Christina S. Winborn & Samantha S. Olah & Carley N. Miller & JungMin Kim & Chelsie A. Kadgien & Hannah S. Actor-Engel & Harrison J. Ramsay & Austin M. Ramsey & Jason Aoto & Matthew J, 2024. "Genetically encoded intrabody probes for labeling and manipulating AMPA-type glutamate receptors," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Christian Keck & Cristina Savin & Jörg Lücke, 2012. "Feedforward Inhibition and Synaptic Scaling – Two Sides of the Same Coin?," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-15, March.
    12. Iris Reuveni & Sourav Ghosh & Edi Barkai, 2017. "Real Time Multiplicative Memory Amplification Mediated by Whole-Cell Scaling of Synaptic Response in Key Neurons," PLOS Computational Biology, Public Library of Science, vol. 13(1), pages 1-31, January.
    13. Jimok Kim & Richard W Tsien & Bradley E Alger, 2012. "An Improved Test for Detecting Multiplicative Homeostatic Synaptic Scaling," PLOS ONE, Public Library of Science, vol. 7(5), pages 1-9, May.
    14. Michael Fauth & Florentin Wörgötter & Christian Tetzlaff, 2015. "The Formation of Multi-synaptic Connections by the Interaction of Synaptic and Structural Plasticity and Their Functional Consequences," PLOS Computational Biology, Public Library of Science, vol. 11(1), pages 1-29, January.
    15. Christoph Hartmann & Andreea Lazar & Bernhard Nessler & Jochen Triesch, 2015. "Where’s the Noise? Key Features of Spontaneous Activity and Neural Variability Arise through Learning in a Deterministic Network," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-35, December.
    16. Julijana Gjorgjieva & Taro Toyoizumi & Stephen J Eglen, 2009. "Burst-Time-Dependent Plasticity Robustly Guides ON/OFF Segregation in the Lateral Geniculate Nucleus," PLOS Computational Biology, Public Library of Science, vol. 5(12), pages 1-19, December.
    17. Mizusaki, Beatriz E.P. & Agnes, Everton J. & Erichsen, Rubem & Brunnet, Leonardo G., 2017. "Learning and retrieval behavior in recurrent neural networks with pre-synaptic dependent homeostatic plasticity," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 479(C), pages 279-286.
    18. Chrisantha Fernando & Vera Vasas & Eörs Szathmáry & Phil Husbands, 2011. "Evolvable Neuronal Paths: A Novel Basis for Information and Search in the Brain," PLOS ONE, Public Library of Science, vol. 6(8), pages 1-24, August.
    19. Glenn N Saxe & Daniel Calderone & Leah J Morales, 2018. "Brain entropy and human intelligence: A resting-state fMRI study," PLOS ONE, Public Library of Science, vol. 13(2), pages 1-21, February.
    20. Giorgia Dellaferrera & Stanisław Woźniak & Giacomo Indiveri & Angeliki Pantazi & Evangelos Eleftheriou, 2022. "Introducing principles of synaptic integration in the optimization of deep neural networks," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0013514. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.