IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47617-6.html
   My bibliography  Save this article

Spontaneous persistent activity and inactivity in vivo reveals differential cortico-entorhinal functional connectivity

Author

Listed:
  • Krishna Choudhary

    (University of California, Los Angeles
    HRL Laboratories)

  • Sven Berberich

    (Heidelberg University
    University Medical Center, Johannes Gutenberg University)

  • Thomas T. G. Hahn

    (Zentralinstitut fur Seelische Gesundheit)

  • James M. McFarland

    (Brown University)

  • Mayank R. Mehta

    (University of California, Los Angeles
    University of California
    University of California
    University of California, Los Angeles)

Abstract

Understanding the functional connectivity between brain regions and its emergent dynamics is a central challenge. Here we present a theory-experiment hybrid approach involving iteration between a minimal computational model and in vivo electrophysiological measurements. Our model not only predicted spontaneous persistent activity (SPA) during Up-Down-State oscillations, but also inactivity (SPI), which has never been reported. These were confirmed in vivo in the membrane potential of neurons, especially from layer 3 of the medial and lateral entorhinal cortices. The data was then used to constrain two free parameters, yielding a unique, experimentally determined model for each neuron. Analytic and computational analysis of the model generated a dozen quantitative predictions about network dynamics, which were all confirmed in vivo to high accuracy. Our technique predicted functional connectivity; e. g. the recurrent excitation is stronger in the medial than lateral entorhinal cortex. This too was confirmed with connectomics data. This technique uncovers how differential cortico-entorhinal dialogue generates SPA and SPI, which could form an energetically efficient working-memory substrate and influence the consolidation of memories during sleep. More broadly, our procedure can reveal the functional connectivity of large networks and a theory of their emergent dynamics.

Suggested Citation

  • Krishna Choudhary & Sven Berberich & Thomas T. G. Hahn & James M. McFarland & Mayank R. Mehta, 2024. "Spontaneous persistent activity and inactivity in vivo reveals differential cortico-entorhinal functional connectivity," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47617-6
    DOI: 10.1038/s41467-024-47617-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47617-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-47617-6?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. Lisa Marshall & Halla Helgadóttir & Matthias Mölle & Jan Born, 2006. "Boosting slow oscillations during sleep potentiates memory," Nature, Nature, vol. 444(7119), pages 610-613, November.
    2. M. R. Mehta & A. K. Lee & M. A. Wilson, 2002. "Role of experience and oscillations in transforming a rate code into a temporal code," Nature, Nature, vol. 417(6890), pages 741-746, June.
    3. Albert Tsao & Jørgen Sugar & Li Lu & Cheng Wang & James J. Knierim & May-Britt Moser & Edvard I. Moser, 2018. "Integrating time from experience in the lateral entorhinal cortex," Nature, Nature, vol. 561(7721), pages 57-62, September.
    4. Torkel Hafting & Marianne Fyhn & Sturla Molden & May-Britt Moser & Edvard I. Moser, 2005. "Microstructure of a spatial map in the entorhinal cortex," Nature, Nature, vol. 436(7052), pages 801-806, August.
    5. Daniel Levenstein & György Buzsáki & John Rinzel, 2019. "NREM sleep in the rodent neocortex and hippocampus reflects excitable dynamics," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    6. Yousheng Shu & Andrea Hasenstaub & David A. McCormick, 2003. "Turning on and off recurrent balanced cortical activity," Nature, Nature, vol. 423(6937), pages 288-293, May.
    7. Mattia Rigotti & Omri Barak & Melissa R. Warden & Xiao-Jing Wang & Nathaniel D. Daw & Earl K. Miller & Stefano Fusi, 2013. "The importance of mixed selectivity in complex cognitive tasks," Nature, Nature, vol. 497(7451), pages 585-590, May.
    8. Alexei V. Egorov & Bassam N. Hamam & Erik Fransén & Michael E. Hasselmo & Angel A. Alonso, 2002. "Graded persistent activity in entorhinal cortex neurons," Nature, Nature, vol. 420(6912), pages 173-178, November.
    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. Qiming Shao & Ligu Chen & Xiaowan Li & Miao Li & Hui Cui & Xiaoyue Li & Xinran Zhao & Yuying Shi & Qiang Sun & Kaiyue Yan & Guangfu Wang, 2024. "A non-canonical visual cortical-entorhinal pathway contributes to spatial navigation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Eleanor Spens & Neil Burgess, 2024. "A generative model of memory construction and consolidation," Nature Human Behaviour, Nature, vol. 8(3), pages 526-543, March.
    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. Kyriaki Sidiropoulou & Panayiota Poirazi, 2012. "Predictive Features of Persistent Activity Emergence in Regular Spiking and Intrinsic Bursting Model Neurons," PLOS Computational Biology, Public Library of Science, vol. 8(4), pages 1-15, April.
    5. Eric Reifenstein & Martin Stemmler & Andreas V M Herz & Richard Kempter & Susanne Schreiber, 2014. "Movement Dependence and Layer Specificity of Entorhinal Phase Precession in Two-Dimensional Environments," PLOS ONE, Public Library of Science, vol. 9(6), pages 1-11, June.
    6. Vanessa F Descalzo & Roberto Gallego & Maria V Sanchez-Vives, 2014. "Adaptation in the Visual Cortex: Influence of Membrane Trajectory and Neuronal Firing Pattern on Slow Afterpotentials," PLOS ONE, Public Library of Science, vol. 9(11), pages 1-10, November.
    7. Florian Raudies & Michael E Hasselmo, 2015. "Differences in Visual-Spatial Input May Underlie Different Compression Properties of Firing Fields for Grid Cell Modules in Medial Entorhinal Cortex," PLOS Computational Biology, Public Library of Science, vol. 11(11), pages 1-27, November.
    8. Ashok Litwin-Kumar & Anne-Marie M Oswald & Nathaniel N Urban & Brent Doiron, 2011. "Balanced Synaptic Input Shapes the Correlation between Neural Spike Trains," PLOS Computational Biology, Public Library of Science, vol. 7(12), pages 1-14, December.
    9. Isabella C. Wagner & Luise P. Graichen & Boryana Todorova & Andre Lüttig & David B. Omer & Matthias Stangl & Claus Lamm, 2023. "Entorhinal grid-like codes and time-locked network dynamics track others navigating through space," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. 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.
    11. Taylor J. Malone & Nai-Wen Tien & Yan Ma & Lian Cui & Shangru Lyu & Garret Wang & Duc Nguyen & Kai Zhang & Maxym V. Myroshnychenko & Jean Tyan & Joshua A. Gordon & David A. Kupferschmidt & Yi Gu, 2024. "A consistent map in the medial entorhinal cortex supports spatial memory," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    12. 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.
    13. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    15. Louis-Emmanuel Martinet & Denis Sheynikhovich & Karim Benchenane & Angelo Arleo, 2011. "Spatial Learning and Action Planning in a Prefrontal Cortical Network Model," PLOS Computational Biology, Public Library of Science, vol. 7(5), pages 1-21, May.
    16. Wenyi Zhang & Yang Xie & Tianming Yang, 2022. "Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    17. Hagai Lalazar & L F Abbott & Eilon Vaadia, 2016. "Tuning Curves for Arm Posture Control in Motor Cortex Are Consistent with Random Connectivity," PLOS Computational Biology, Public Library of Science, vol. 12(5), pages 1-27, May.
    18. Xiaxia Xu & Lingzhen Song & Rebecca Kringel & Ileana L. Hanganu-Opatz, 2021. "Developmental decrease of entorhinal-hippocampal communication in immune-challenged DISC1 knockdown mice," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    19. Dhanya Parameshwaran & Upinder S Bhalla, 2013. "Theta Frequency Background Tunes Transmission but Not Summation of Spiking Responses," PLOS ONE, Public Library of Science, vol. 8(1), pages 1-12, January.
    20. Alexander Thomas Keinath, 2016. "The Preferred Directions of Conjunctive Grid X Head Direction Cells in the Medial Entorhinal Cortex Are Periodically Organized," PLOS ONE, Public Library of Science, vol. 11(3), pages 1-11, March.

    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_s41467-024-47617-6. 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.