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

Author

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  • 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
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    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. David Stellwagen & Robert C. Malenka, 2006. "Synaptic scaling mediated by glial TNF-α," Nature, Nature, vol. 440(7087), pages 1054-1059, April.
    10. 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.
    11. 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.
    12. 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.
    13. 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.
    14. 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.
    15. Christopher D. Harvey & Karel Svoboda, 2007. "Locally dynamic synaptic learning rules in pyramidal neuron dendrites," Nature, Nature, vol. 450(7173), pages 1195-1200, December.
    16. Joseph Cichon & Wen-Biao Gan, 2015. "Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity," Nature, Nature, vol. 520(7546), pages 180-185, April.
    Full references (including those not matched with items on IDEAS)

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