IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47571-3.html
   My bibliography  Save this article

Intracellular magnesium optimizes transmission efficiency and plasticity of hippocampal synapses by reconfiguring their connectivity

Author

Listed:
  • Hang Zhou

    (Shenzhen University of Advanced Technology
    Chinese Academy of Sciences)

  • Guo-Qiang Bi

    (Shenzhen University of Advanced Technology
    Chinese Academy of Sciences
    Shenzhen-Hong Kong Institute of Brain Science
    University of Science and Technology of China)

  • Guosong Liu

    (Tsinghua University
    NeuroCentria Inc.)

Abstract

Synapses at dendritic branches exhibit specific properties for information processing. However, how the synapses are orchestrated to dynamically modify their properties, thus optimizing information processing, remains elusive. Here, we observed at hippocampal dendritic branches diverse configurations of synaptic connectivity, two extremes of which are characterized by low transmission efficiency, high plasticity and coding capacity, or inversely. The former favors information encoding, pertinent to learning, while the latter prefers information storage, relevant to memory. Presynaptic intracellular Mg2+ crucially mediates the dynamic transition continuously between the two extreme configurations. Consequently, varying intracellular Mg2+ levels endow individual branches with diverse synaptic computations, thus modulating their ability to process information. Notably, elevating brain Mg2+ levels in aging animals restores synaptic configuration resembling that of young animals, coincident with improved learning and memory. These findings establish intracellular Mg2+ as a crucial factor reconfiguring synaptic connectivity at dendrites, thus optimizing their branch-specific properties in information processing.

Suggested Citation

  • Hang Zhou & Guo-Qiang Bi & Guosong Liu, 2024. "Intracellular magnesium optimizes transmission efficiency and plasticity of hippocampal synapses by reconfiguring their connectivity," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47571-3
    DOI: 10.1038/s41467-024-47571-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47571-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-47571-3?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. Wei-Chung Allen Lee & Vincent Bonin & Michael Reed & Brett J. Graham & Greg Hood & Katie Glattfelder & R. Clay Reid, 2016. "Anatomy and function of an excitatory network in the visual cortex," Nature, Nature, vol. 532(7599), pages 370-374, April.
    2. Maria Lavzin & Sophia Rapoport & Alon Polsky & Liora Garion & Jackie Schiller, 2012. "Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo," Nature, Nature, vol. 490(7420), pages 397-401, October.
    3. David Stellwagen & Robert C. Malenka, 2006. "Synaptic scaling mediated by glial TNF-α," Nature, Nature, vol. 440(7087), pages 1054-1059, April.
    4. Akiko Hayashi-Takagi & Sho Yagishita & Mayumi Nakamura & Fukutoshi Shirai & Yi I. Wu & Amanda L. Loshbaugh & Brian Kuhlman & Klaus M. Hahn & Haruo Kasai, 2015. "Labelling and optical erasure of synaptic memory traces in the motor cortex," Nature, Nature, vol. 525(7569), pages 333-338, September.
    5. Ning-long Xu & Mark T. Harnett & Stephen R. Williams & Daniel Huber & Daniel H. O’Connor & Karel Svoboda & Jeffrey C. Magee, 2012. "Nonlinear dendritic integration of sensory and motor input during an active sensing task," Nature, Nature, vol. 492(7428), pages 247-251, December.
    6. Kirill Grushin & Jing Wang & Jeff Coleman & James E. Rothman & Charles V. Sindelar & Shyam S. Krishnakumar, 2019. "Structural basis for the clamping and Ca2+ activation of SNARE-mediated fusion by synaptotagmin," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    7. Jackie Schiller & Guy Major & Helmut J. Koester & Yitzhak Schiller, 2000. "NMDA spikes in basal dendrites of cortical pyramidal neurons," Nature, Nature, vol. 404(6775), pages 285-289, March.
    8. Joseph Cichon & Wen-Biao Gan, 2015. "Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity," Nature, Nature, vol. 520(7546), pages 180-185, April.
    9. Sébastien Royer & Denis Paré, 2003. "Conservation of total synaptic weight through balanced synaptic depression and potentiation," Nature, Nature, vol. 422(6931), pages 518-522, April.
    10. Attila Losonczy & Judit K. Makara & Jeffrey C. Magee, 2008. "Compartmentalized dendritic plasticity and input feature storage in neurons," Nature, Nature, vol. 452(7186), pages 436-441, March.
    11. Lu Chen & Dane M. Chetkovich & Ronald S. Petralia & Neal T. Sweeney & Yoshimi Kawasaki & Robert J. Wenthold & David S. Bredt & Roger A. Nicoll, 2000. "Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms," Nature, Nature, vol. 408(6815), pages 936-943, December.
    12. M. Florencia Iacaruso & Ioana T. Gasler & Sonja B. Hofer, 2017. "Synaptic organization of visual space in primary visual cortex," Nature, Nature, vol. 547(7664), pages 449-452, July.
    13. Spencer L. Smith & Ikuko T. Smith & Tiago Branco & Michael Häusser, 2013. "Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo," Nature, Nature, vol. 503(7474), pages 115-120, November.
    14. Lee Cossell & Maria Florencia Iacaruso & Dylan R. Muir & Rachael Houlton & Elie N. Sader & Ho Ko & Sonja B. Hofer & Thomas D. Mrsic-Flogel, 2015. "Functional organization of excitatory synaptic strength in primary visual cortex," Nature, Nature, vol. 518(7539), pages 399-403, February.
    15. Simone Holler & German Köstinger & Kevan A. C. Martin & Gregor F. P. Schuhknecht & Ken J. Stratford, 2021. "Structure and function of a neocortical synapse," Nature, Nature, vol. 591(7848), pages 111-116, March.
    16. Christopher D. Harvey & Karel Svoboda, 2007. "Locally dynamic synaptic learning rules in pyramidal neuron dendrites," Nature, Nature, vol. 450(7173), pages 1195-1200, December.
    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. Matteo Farinella & Daniel T Ruedt & Padraig Gleeson & Frederic Lanore & R Angus Silver, 2014. "Glutamate-Bound NMDARs Arising from In Vivo-like Network Activity Extend Spatio-temporal Integration in a L5 Cortical Pyramidal Cell Model," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-21, April.
    2. Linda Judák & Balázs Chiovini & Gábor Juhász & Dénes Pálfi & Zsolt Mezriczky & Zoltán Szadai & Gergely Katona & Benedek Szmola & Katalin Ócsai & Bernadett Martinecz & Anna Mihály & Ádám Dénes & Bálint, 2022. "Sharp-wave ripple doublets induce complex dendritic spikes in parvalbumin interneurons in vivo," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Balázs Ujfalussy & Tamás Kiss & Péter Érdi, 2009. "Parallel Computational Subunits in Dentate Granule Cells Generate Multiple Place Fields," PLOS Computational Biology, Public Library of Science, vol. 5(9), pages 1-16, September.
    4. Stefano Recanatesi & Gabriel Koch Ocker & Michael A Buice & Eric Shea-Brown, 2019. "Dimensionality in recurrent spiking networks: Global trends in activity and local origins in connectivity," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-29, July.
    5. Bettina Voelcker & Ravi Pancholi & Simon Peron, 2022. "Transformation of primary sensory cortical representations from layer 4 to layer 2," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Carles Bosch & Tobias Ackels & Alexandra Pacureanu & Yuxin Zhang & Christopher J. Peddie & Manuel Berning & Norman Rzepka & Marie-Christine Zdora & Isabell Whiteley & Malte Storm & Anne Bonnin & Chris, 2022. "Functional and multiscale 3D structural investigation of brain tissue through correlative in vivo physiology, synchrotron microtomography and volume electron microscopy," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Zhou, Xinjia & Zhang, Yan & Gu, Tianyi & Zheng, Muhua & Xu, Kesheng, 2024. "Mixed synaptic modulation and inhibitory plasticity perform complementary roles in metastable transitions," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 635(C).
    8. Bartul Mimica & Tuçe Tombaz & Claudia Battistin & Jingyi Guo Fuglstad & Benjamin A. Dunn & Jonathan R. Whitlock, 2023. "Behavioral decomposition reveals rich encoding structure employed across neocortex in rats," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    9. Yichen Zhang & Gan He & Lei Ma & Xiaofei Liu & J. J. Johannes Hjorth & Alexander Kozlov & Yutao He & Shenjian Zhang & Jeanette Hellgren Kotaleski & Yonghong Tian & Sten Grillner & Kai Du & Tiejun Huan, 2023. "A GPU-based computational framework that bridges neuron simulation and artificial intelligence," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. Yoav Printz & Pritish Patil & Mathias Mahn & Asaf Benjamin & Anna Litvin & Rivka Levy & Max Bringmann & Ofer Yizhar, 2023. "Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Zhiwei Xu & Erez Geron & Luis M. Pérez-Cuesta & Yang Bai & Wen-Biao Gan, 2023. "Generalized extinction of fear memory depends on co-allocation of synaptic plasticity in dendrites," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Gabriel Koch Ocker & Krešimir Josić & Eric Shea-Brown & Michael A Buice, 2017. "Linking structure and activity in nonlinear spiking networks," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-47, June.
    13. Wen-Hao Zhang & Si Wu & Krešimir Josić & Brent Doiron, 2023. "Sampling-based Bayesian inference in recurrent circuits of stochastic spiking neurons," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. 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.
    15. Francesco Paolo Ulloa Severino & Oluwadamilola O. Lawal & Kristina Sakers & Shiyi Wang & Namsoo Kim & Alexander David Friedman & Sarah Anne Johnson & Chaichontat Sriworarat & Ryan H. Hughes & Scott H., 2023. "Training-induced circuit-specific excitatory synaptogenesis in mice is required for effort control," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    16. Jérémie Sibille & Carolin Gehr & Jonathan I. Benichov & Hymavathy Balasubramanian & Kai Lun Teh & Tatiana Lupashina & Daniela Vallentin & Jens Kremkow, 2022. "High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    17. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Yifan Gu & Yang Qi & Pulin Gong, 2019. "Rich-club connectivity, diverse population coupling, and dynamical activity patterns emerging from local cortical circuits," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-34, April.
    19. Shan Shen & Xiaolong Jiang & Federico Scala & Jiakun Fu & Paul Fahey & Dmitry Kobak & Zhenghuan Tan & Na Zhou & Jacob Reimer & Fabian Sinz & Andreas S. Tolias, 2022. "Distinct organization of two cortico-cortical feedback pathways," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    20. Vardi, Roni & Tugendhaft, Yael & Kanter, Ido, 2023. "Neuronal plasticity features are independent of neuronal holding membrane potential," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 632(P1).

    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:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47571-3. 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: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    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.