IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34520-1.html
   My bibliography  Save this article

Sharp-wave ripple doublets induce complex dendritic spikes in parvalbumin interneurons in vivo

Author

Listed:
  • Linda Judák

    (Institute of Experimental Medicine)

  • Balázs Chiovini

    (Institute of Experimental Medicine
    Pázmány Péter University)

  • Gábor Juhász

    (Pázmány Péter University)

  • Dénes Pálfi

    (Institute of Experimental Medicine
    Pázmány Péter University)

  • Zsolt Mezriczky

    (Pázmány Péter University)

  • Zoltán Szadai

    (Institute of Experimental Medicine)

  • Gergely Katona

    (Pázmány Péter University)

  • Benedek Szmola

    (Pázmány Péter University)

  • Katalin Ócsai

    (Pázmány Péter University)

  • Bernadett Martinecz

    (Institute of Experimental Medicine)

  • Anna Mihály

    (Pázmány Péter University)

  • Ádám Dénes

    (Institute of Experimental Medicine)

  • Bálint Kerekes

    (Pázmány Péter University
    Research Centre for Natural Sciences)

  • Áron Szepesi

    (Institute of Experimental Medicine)

  • Gergely Szalay

    (Institute of Experimental Medicine)

  • István Ulbert

    (Pázmány Péter University
    Research Centre for Natural Sciences)

  • Zoltán Mucsi

    (BrainVisionCenter)

  • Botond Roska

    (BrainVisionCenter
    Institute of Molecular and Clinical Ophthalmology Basel
    Friedrich Miescher Institute
    University of Basel)

  • Balázs Rózsa

    (Institute of Experimental Medicine
    Pázmány Péter University
    BrainVisionCenter)

Abstract

Neuronal plasticity has been shown to be causally linked to coincidence detection through dendritic spikes (dSpikes). We demonstrate the existence of SPW-R-associated, branch-specific, local dSpikes and their computational role in basal dendrites of hippocampal PV+ interneurons in awake animals. To measure the entire dendritic arbor of long thin dendrites during SPW-Rs, we used fast 3D acousto-optical imaging through an eccentric deep-brain adapter and ipsilateral local field potential recording. The regenerative calcium spike started at variable, NMDA-AMPA-dependent, hot spots and propagated in both direction with a high amplitude beyond a critical distance threshold (~150 µm) involving voltage-gated calcium channels. A supralinear dendritic summation emerged during SPW-R doublets when two successive SPW-R events coincide within a short temporal window (~150 ms), e.g., during more complex association tasks, and generated large dSpikes with an about 2.5-3-fold amplitude increase which propagated down to the soma. Our results suggest that these doublet-associated dSpikes can work as a dendritic-level temporal and spatial coincidence detector during SPW-R-related network computation in awake mice.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34520-1
    DOI: 10.1038/s41467-022-34520-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34520-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-34520-1?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. 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.
    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. David J. Foster & Matthew A. Wilson, 2006. "Reverse replay of behavioural sequences in hippocampal place cells during the awake state," Nature, Nature, vol. 440(7084), pages 680-683, March.
    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. Joseph Cichon & Wen-Biao Gan, 2015. "Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity," Nature, Nature, vol. 520(7546), pages 180-185, April.
    6. Alexandra Tzilivaki & George Kastellakis & Panayiota Poirazi, 2019. "Challenging the point neuron dogma: FS basket cells as 2-stage nonlinear integrators," Nature Communications, Nature, vol. 10(1), pages 1-14, 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. 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.
    2. 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.
    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. Zhenrui Liao & Kevin C. Gonzalez & Deborah M. Li & Catalina M. Yang & Donald Holder & Natalie E. McClain & Guofeng Zhang & Stephen W. Evans & Mariya Chavarha & Jane Simko & Christopher D. Makinson & M, 2024. "Functional architecture of intracellular oscillations in hippocampal dendrites," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Hanle Zheng & Zhong Zheng & Rui Hu & Bo Xiao & Yujie Wu & Fangwen Yu & Xue Liu & Guoqi Li & Lei Deng, 2024. "Temporal dendritic heterogeneity incorporated with spiking neural networks for learning multi-timescale dynamics," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. J Matthew Mahoney & Ali S Titiz & Amanda E Hernan & Rod C Scott, 2016. "Short-Range Temporal Interactions in Sleep; Hippocampal Spike Avalanches Support a Large Milieu of Sequential Activity Including Replay," PLOS ONE, Public Library of Science, vol. 11(2), pages 1-25, February.
    7. Marta Huelin Gorriz & Masahiro Takigawa & Daniel Bendor, 2023. "The role of experience in prioritizing hippocampal replay," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Nicolas Cazin & Martin Llofriu Alonso & Pablo Scleidorovich Chiodi & Tatiana Pelc & Bruce Harland & Alfredo Weitzenfeld & Jean-Marc Fellous & Peter Ford Dominey, 2019. "Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-32, July.
    9. Nozomu H. Nakamura & Hidemasa Furue & Kenta Kobayashi & Yoshitaka Oku, 2023. "Hippocampal ensemble dynamics and memory performance are modulated by respiration during encoding," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Usman Farooq & George Dragoi, 2024. "Experience of Euclidean geometry sculpts the development and dynamics of rodent hippocampal sequential cell assemblies," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    11. 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.
    12. Chaogan Yan & Dongqiang Liu & Yong He & Qihong Zou & Chaozhe Zhu & Xinian Zuo & Xiangyu Long & Yufeng Zang, 2009. "Spontaneous Brain Activity in the Default Mode Network Is Sensitive to Different Resting-State Conditions with Limited Cognitive Load," PLOS ONE, Public Library of Science, vol. 4(5), pages 1-11, May.
    13. 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.
    14. Asako Noguchi & Roman Huszár & Shota Morikawa & György Buzsáki & Yuji Ikegaya, 2022. "Inhibition allocates spikes during hippocampal ripples," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    15. Zhewei Zhang & Yuji K. Takahashi & Marlian Montesinos-Cartegena & Thorsten Kahnt & Angela J. Langdon & Geoffrey Schoenbaum, 2024. "Expectancy-related changes in firing of dopamine neurons depend on hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    16. Anli A. Liu & Simon Henin & Saman Abbaspoor & Anatol Bragin & Elizabeth A. Buffalo & Jordan S. Farrell & David J. Foster & Loren M. Frank & Tamara Gedankien & Jean Gotman & Jennifer A. Guidera & Kari , 2022. "A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. 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.
    18. Carina Curto & Vladimir Itskov, 2008. "Cell Groups Reveal Structure of Stimulus Space," PLOS Computational Biology, Public Library of Science, vol. 4(10), pages 1-13, October.
    19. Dejan Pecevski & Lars Buesing & Wolfgang Maass, 2011. "Probabilistic Inference in General Graphical Models through Sampling in Stochastic Networks of Spiking Neurons," PLOS Computational Biology, Public Library of Science, vol. 7(12), pages 1-25, December.
    20. Will D Penny & Peter Zeidman & Neil Burgess, 2013. "Forward and Backward Inference in Spatial Cognition," PLOS Computational Biology, Public Library of Science, vol. 9(12), pages 1-22, 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_s41467-022-34520-1. 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.