IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0115764.html
   My bibliography  Save this article

Multiplex Networks of Cortical and Hippocampal Neurons Revealed at Different Timescales

Author

Listed:
  • Nicholas Timme
  • Shinya Ito
  • Maxym Myroshnychenko
  • Fang-Chin Yeh
  • Emma Hiolski
  • Pawel Hottowy
  • John M Beggs

Abstract

Recent studies have emphasized the importance of multiplex networks – interdependent networks with shared nodes and different types of connections – in systems primarily outside of neuroscience. Though the multiplex properties of networks are frequently not considered, most networks are actually multiplex networks and the multiplex specific features of networks can greatly affect network behavior (e.g. fault tolerance). Thus, the study of networks of neurons could potentially be greatly enhanced using a multiplex perspective. Given the wide range of temporally dependent rhythms and phenomena present in neural systems, we chose to examine multiplex networks of individual neurons with time scale dependent connections. To study these networks, we used transfer entropy – an information theoretic quantity that can be used to measure linear and nonlinear interactions – to systematically measure the connectivity between individual neurons at different time scales in cortical and hippocampal slice cultures. We recorded the spiking activity of almost 12,000 neurons across 60 tissue samples using a 512-electrode array with 60 micrometer inter-electrode spacing and 50 microsecond temporal resolution. To the best of our knowledge, this preparation and recording method represents a superior combination of number of recorded neurons and temporal and spatial recording resolutions to any currently available in vivo system. We found that highly connected neurons (“hubs”) were localized to certain time scales, which, we hypothesize, increases the fault tolerance of the network. Conversely, a large proportion of non-hub neurons were not localized to certain time scales. In addition, we found that long and short time scale connectivity was uncorrelated. Finally, we found that long time scale networks were significantly less modular and more disassortative than short time scale networks in both tissue types. As far as we are aware, this analysis represents the first systematic study of temporally dependent multiplex networks among individual neurons.

Suggested Citation

  • Nicholas Timme & Shinya Ito & Maxym Myroshnychenko & Fang-Chin Yeh & Emma Hiolski & Pawel Hottowy & John M Beggs, 2014. "Multiplex Networks of Cortical and Hippocampal Neurons Revealed at Different Timescales," PLOS ONE, Public Library of Science, vol. 9(12), pages 1-43, December.
    • Handle: RePEc:plo:pone00:0115764
    DOI: 10.1371/journal.pone.0115764
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0115764
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0115764&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0115764?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. Alexander Nakhnikian & George V Rebec & Leslie M Grasse & Lucas L Dwiel & Masanori Shimono & John M Beggs, 2014. "Behavior Modulates Effective Connectivity between Cortex and Striatum," PLOS ONE, Public Library of Science, vol. 9(3), pages 1-14, March.
    2. Sergey V. Buldyrev & Roni Parshani & Gerald Paul & H. Eugene Stanley & Shlomo Havlin, 2010. "Catastrophic cascade of failures in interdependent networks," Nature, Nature, vol. 464(7291), pages 1025-1028, April.
    3. Shinya Ito & Fang-Chin Yeh & Emma Hiolski & Przemyslaw Rydygier & Deborah E Gunning & Pawel Hottowy & Nicholas Timme & Alan M Litke & John M Beggs, 2014. "Large-Scale, High-Resolution Multielectrode-Array Recording Depicts Functional Network Differences of Cortical and Hippocampal Cultures," PLOS ONE, Public Library of Science, vol. 9(8), pages 1-16, August.
    4. Michael Wibral & Nicolae Pampu & Viola Priesemann & Felix Siebenhühner & Hannes Seiwert & Michael Lindner & Joseph T Lizier & Raul Vicente, 2013. "Measuring Information-Transfer Delays," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-19, February.
    5. Patricia Wollstadt & Mario Martínez-Zarzuela & Raul Vicente & Francisco J Díaz-Pernas & Michael Wibral, 2014. "Efficient Transfer Entropy Analysis of Non-Stationary Neural Time Series," PLOS ONE, Public Library of Science, vol. 9(7), pages 1-21, July.
    6. Granger, C W J, 1969. "Investigating Causal Relations by Econometric Models and Cross-Spectral Methods," Econometrica, Econometric Society, vol. 37(3), pages 424-438, July.
    7. Shinya Ito & Michael E Hansen & Randy Heiland & Andrew Lumsdaine & Alan M Litke & John M Beggs, 2011. "Extending Transfer Entropy Improves Identification of Effective Connectivity in a Spiking Cortical Network Model," PLOS ONE, Public Library of Science, vol. 6(11), pages 1-13, 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. Zanin, Massimiliano, 2015. "Can we neglect the multi-layer structure of functional networks?," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 430(C), pages 184-192.
    2. Xiaogeng Wan & Lanxi Xu, 2018. "A study for multiscale information transfer measures based on conditional mutual information," PLOS ONE, Public Library of Science, vol. 13(12), pages 1-30, December.
    3. Shinya Ito & Fang-Chin Yeh & Emma Hiolski & Przemyslaw Rydygier & Deborah E Gunning & Pawel Hottowy & Nicholas Timme & Alan M Litke & John M Beggs, 2014. "Large-Scale, High-Resolution Multielectrode-Array Recording Depicts Functional Network Differences of Cortical and Hippocampal Cultures," PLOS ONE, Public Library of Science, vol. 9(8), pages 1-16, August.
    4. Leonidas Sandoval Junior & Asher Mullokandov & Dror Y. Kenett, 2015. "Dependency Relations among International Stock Market Indices," JRFM, MDPI, vol. 8(2), pages 1-39, May.
    5. Huynh, Toan Luu Duc & Nasir, Muhammad Ali & Vo, Xuan Vinh & Nguyen, Thong Trung, 2020. "“Small things matter most”: The spillover effects in the cryptocurrency market and gold as a silver bullet," The North American Journal of Economics and Finance, Elsevier, vol. 54(C).
    6. Yonathan Murin & Jeremy Kim & Josef Parvizi & Andrea Goldsmith, 2018. "SozRank: A new approach for localizing the epileptic seizure onset zone," PLOS Computational Biology, Public Library of Science, vol. 14(1), pages 1-26, January.
    7. Emeka Nkoro & Aham Kelvin Uko, 2016. "Exchange Rate and Inflation Volatility and Stock Prices Volatility: Evidence from Nigeria, 1986-2012," Journal of Applied Finance & Banking, SCIENPRESS Ltd, vol. 6(6), pages 1-4.
    8. Czujack, Corinna & Flôres Junior, Renato Galvão & Ginsburgh, Victor, 1995. "On long-run price comovements between paintings and prints," FGV EPGE Economics Working Papers (Ensaios Economicos da EPGE) 269, EPGE Brazilian School of Economics and Finance - FGV EPGE (Brazil).
    9. Bier, Vicki & Gutfraind, Alexander, 2019. "Risk analysis beyond vulnerability and resilience – characterizing the defensibility of critical systems," European Journal of Operational Research, Elsevier, vol. 276(2), pages 626-636.
    10. Sotirios Varelas, 2022. "Virtual Immersive Platforms as a Strategic Innovative Destination Marketing Tool in the COVID-19 Era," Sustainability, MDPI, vol. 14(19), pages 1-15, October.
    11. Loperfido, Nicola, 2010. "A note on marginal and conditional independence," Statistics & Probability Letters, Elsevier, vol. 80(23-24), pages 1695-1699, December.
    12. Hyunsoo Kang, 2022. "Impacts of Income Inequality and Economic Growth on CO 2 Emissions: Comparing the Gini Coefficient and the Top Income Share in OECD Countries," Energies, MDPI, vol. 15(19), pages 1-15, September.
    13. KAMKOUM, Arnaud Cedric, 2023. "The Federal Reserve’s Response to the Global Financial Crisis and its Effects: An Interrupted Time-Series Analysis of the Impact of its Quantitative Easing Programs," Thesis Commons d7pvg, Center for Open Science.
    14. Bierens, H.J. & Broersma, L., 1991. "The relation between unemployment and interest rate : some international evidence," Serie Research Memoranda 0112, VU University Amsterdam, Faculty of Economics, Business Administration and Econometrics.
    15. Zamani, Mehrzad, 2007. "Energy consumption and economic activities in Iran," Energy Economics, Elsevier, vol. 29(6), pages 1135-1140, November.
    16. Jumah, Adusei & Kunst, Robert M., 2001. "The Effects of Exchange-Rate Exposures on Equity Asset Markets," Economics Series 94, Institute for Advanced Studies.
    17. Muhammad Shafiullah & Ravinthirakumaran Navaratnam, 2016. "Do Bangladesh and Sri Lanka Enjoy Export-Led Growth? A Comparison of Two Small South Asian Economies," South Asia Economic Journal, Institute of Policy Studies of Sri Lanka, vol. 17(1), pages 114-132, March.
    18. Portes, Richard & Santorum, Anita, 1987. "Money and the consumption goods market in China," Journal of Comparative Economics, Elsevier, vol. 11(3), pages 354-371, September.
    19. Alberto Fuertes & Simón Sosvilla-Rivero, 2019. "“Forecasting emerging market currencies: Are inflation expectations useful?”," IREA Working Papers 201918, University of Barcelona, Research Institute of Applied Economics, revised Oct 2019.
    20. Diana Ricciulli-Marín, 2020. "The Fiscal Cost of Conflict: Evidence from La Violencia in Colombia," Cuadernos de Historia Económica 53, Banco de la Republica de Colombia.

    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:plo:pone00:0115764. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.