IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35620-8.html
   My bibliography  Save this article

An astrocytic signaling loop for frequency-dependent control of dendritic integration and spatial learning

Author

Listed:
  • Kirsten Bohmbach

    (University of Bonn)

  • Nicola Masala

    (University of Bonn)

  • Eva M. Schönhense

    (University of Bonn)

  • Katharina Hill

    (University of Bonn)

  • André N. Haubrich

    (University of Bonn)

  • Andreas Zimmer

    (University of Bonn)

  • Thoralf Opitz

    (University of Bonn)

  • Heinz Beck

    (University of Bonn
    German Center for Neurodegenerative Diseases (DZNE))

  • Christian Henneberger

    (University of Bonn
    German Center for Neurodegenerative Diseases (DZNE)
    University College London)

Abstract

Dendrites of hippocampal CA1 pyramidal cells amplify clustered glutamatergic input by activation of voltage-gated sodium channels and N-methyl-D-aspartate receptors (NMDARs). NMDAR activity depends on the presence of NMDAR co-agonists such as D-serine, but how co-agonists influence dendritic integration is not well understood. Using combinations of whole-cell patch clamp, iontophoretic glutamate application, two-photon excitation fluorescence microscopy and glutamate uncaging in acute rat and mouse brain slices we found that exogenous D-serine reduced the threshold of dendritic spikes and increased their amplitude. Triggering an astrocytic mechanism controlling endogenous D-serine supply via endocannabinoid receptors (CBRs) also increased dendritic spiking. Unexpectedly, this pathway was activated by pyramidal cell activity primarily in the theta range, which required HCN channels and astrocytic CB1Rs. Therefore, astrocytes close a positive and frequency-dependent feedback loop between pyramidal cell activity and their integration of dendritic input. Its disruption in mice led to an impairment of spatial memory, which demonstrated its behavioral relevance.

Suggested Citation

  • Kirsten Bohmbach & Nicola Masala & Eva M. Schönhense & Katharina Hill & André N. Haubrich & Andreas Zimmer & Thoralf Opitz & Heinz Beck & Christian Henneberger, 2022. "An astrocytic signaling loop for frequency-dependent control of dendritic integration and spatial learning," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35620-8
    DOI: 10.1038/s41467-022-35620-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35620-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35620-8?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. Daniel Jimenez-Blasco & Arnau Busquets-Garcia & Etienne Hebert-Chatelain & Roman Serrat & Carlos Vicente-Gutierrez & Christina Ioannidou & Paula Gómez-Sotres & Irene Lopez-Fabuel & Monica Resch-Beushe, 2020. "Glucose metabolism links astroglial mitochondria to cannabinoid effects," Nature, Nature, vol. 583(7817), pages 603-608, July.
    2. Christian Henneberger & Thomas Papouin & Stéphane H. R. Oliet & Dmitri A. Rusakov, 2010. "Long-term potentiation depends on release of d-serine from astrocytes," Nature, Nature, vol. 463(7278), pages 232-236, January.
    3. Christopher D. Harvey & Forrest Collman & Daniel A. Dombeck & David W. Tank, 2009. "Intracellular dynamics of hippocampal place cells during virtual navigation," Nature, Nature, vol. 461(7266), pages 941-946, October.
    4. 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.
    5. Adi Doron & Alon Rubin & Aviya Benmelech-Chovav & Netai Benaim & Tom Carmi & Ron Refaeli & Nechama Novick & Tirzah Kreisel & Yaniv Ziv & Inbal Goshen, 2022. "Hippocampal astrocytes encode reward location," Nature, Nature, vol. 609(7928), pages 772-778, September.
    6. Mark E. J. Sheffield & Daniel A. Dombeck, 2015. "Calcium transient prevalence across the dendritic arbour predicts place field properties," Nature, Nature, vol. 517(7533), pages 200-204, January.
    7. Nephi Stella & Paul Schweitzer & Daniele Piomelli, 1997. "A second endogenous cannabinoid that modulates long-term potentiation," Nature, Nature, vol. 388(6644), pages 773-778, August.
    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. Nathan Fearby & Samantha Penman & Panayotis Thanos, 2022. "Effects of Δ9-Tetrahydrocannibinol (THC) on Obesity at Different Stages of Life: A Literature Review," IJERPH, MDPI, vol. 19(6), pages 1-28, March.
    2. Nicola Forte & Serena Boccella & Lea Tunisi & Alba Clara Fernández-Rilo & Roberta Imperatore & Fabio Arturo Iannotti & Maria Risi & Monica Iannotta & Fabiana Piscitelli & Raffaele Capasso & Paolo Giro, 2021. "Orexin-A and endocannabinoids are involved in obesity-associated alteration of hippocampal neurogenesis, plasticity, and episodic memory in mice," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    3. 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.
    4. Yung-Tian A. Gau & Eric T. Hsu & Richard J. Cha & Rebecca W. Pak & Loren L. Looger & Jin U. Kang & Dwight E. Bergles, 2024. "Multicore fiber optic imaging reveals that astrocyte calcium activity in the mouse cerebral cortex is modulated by internal motivational state," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    5. David J Marcus & Angela N Henderson-Redmond & Maciej Gonek & Michael L Zee & Jill C Farnsworth & Randa A Amin & Mary-Jeanette Andrews & Brian J Davis & Ken Mackie & Daniel J Morgan, 2017. "Mice expressing a “hyper-sensitive” form of the CB1 cannabinoid receptor (CB1) show modestly enhanced alcohol preference and consumption," PLOS ONE, Public Library of Science, vol. 12(4), pages 1-17, April.
    6. Yuto Hasegawa & Juhyun Kim & Gianluca Ursini & Yan Jouroukhin & Xiaolei Zhu & Yu Miyahara & Feiyi Xiong & Samskruthi Madireddy & Mizuho Obayashi & Beat Lutz & Akira Sawa & Solange P. Brown & Mikhail V, 2023. "Microglial cannabinoid receptor type 1 mediates social memory deficits in mice produced by adolescent THC exposure and 16p11.2 duplication," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Shinichiro Kira & Houman Safaai & Ari S. Morcos & Stefano Panzeri & Christopher D. Harvey, 2023. "A distributed and efficient population code of mixed selectivity neurons for flexible navigation decisions," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    8. Eric Lowet & Krishnakanth Kondabolu & Samuel Zhou & Rebecca A. Mount & Yangyang Wang & Cara R. Ravasio & Xue Han, 2022. "Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Marta Gómez-Gonzalo & Gabriele Losi & Angela Chiavegato & Micaela Zonta & Mario Cammarota & Marco Brondi & Francesco Vetri & Laura Uva & Tullio Pozzan & Marco de Curtis & Gian Michele Ratto & Giorgio , 2010. "An Excitatory Loop with Astrocytes Contributes to Drive Neurons to Seizure Threshold," PLOS Biology, Public Library of Science, vol. 8(4), pages 1-19, April.
    10. 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.
    11. Seetha Krishnan & Chad Heer & Chery Cherian & Mark E. J. Sheffield, 2022. "Reward expectation extinction restructures and degrades CA1 spatial maps through loss of a dopaminergic reward proximity signal," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    12. 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.
    13. 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.
    14. Florian Raudies & Michael E Hasselmo, 2012. "Modeling Boundary Vector Cell Firing Given Optic Flow as a Cue," PLOS Computational Biology, Public Library of Science, vol. 8(6), pages 1-17, June.
    15. David M Santucci & Sridhar Raghavachari, 2008. "The Effects of NR2 Subunit-Dependent NMDA Receptor Kinetics on Synaptic Transmission and CaMKII Activation," PLOS Computational Biology, Public Library of Science, vol. 4(10), pages 1-16, October.
    16. Thibault Cholvin & Marlene Bartos, 2022. "Hemisphere-specific spatial representation by hippocampal granule cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. Albert Stuart Reece & Gary Kenneth Hulse, 2022. "Epigenomic and Other Evidence for Cannabis-Induced Aging Contextualized in a Synthetic Epidemiologic Overview of Cannabinoid-Related Teratogenesis and Cannabinoid-Related Carcinogenesis," IJERPH, MDPI, vol. 19(24), pages 1-57, December.
    18. Brent Kevin Young & Jayden Nicole Brennan & Ping Wang & Ning Tian, 2018. "Virtual reality method to analyze visual recognition in mice," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-14, May.
    19. Erkan, Erdem, 2023. "Signal encoding performance of astrocyte-dressed Morris Lecar neurons," Chaos, Solitons & Fractals, Elsevier, vol. 177(C).
    20. Adam Institoris & Milène Vandal & Govind Peringod & Christy Catalano & Cam Ha Tran & Xinzhu Yu & Frank Visser & Cheryl Breiteneder & Leonardo Molina & Baljit S. Khakh & Minh Dang Nguyen & Roger J. Tho, 2022. "Astrocytes amplify neurovascular coupling to sustained activation of neocortex in awake mice," Nature Communications, Nature, vol. 13(1), pages 1-17, 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:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35620-8. 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.