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How Structure Determines Correlations in Neuronal Networks

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  • Volker Pernice
  • Benjamin Staude
  • Stefano Cardanobile
  • Stefan Rotter

Abstract

Networks are becoming a ubiquitous metaphor for the understanding of complex biological systems, spanning the range between molecular signalling pathways, neural networks in the brain, and interacting species in a food web. In many models, we face an intricate interplay between the topology of the network and the dynamics of the system, which is generally very hard to disentangle. A dynamical feature that has been subject of intense research in various fields are correlations between the noisy activity of nodes in a network. We consider a class of systems, where discrete signals are sent along the links of the network. Such systems are of particular relevance in neuroscience, because they provide models for networks of neurons that use action potentials for communication. We study correlations in dynamic networks with arbitrary topology, assuming linear pulse coupling. With our novel approach, we are able to understand in detail how specific structural motifs affect pairwise correlations. Based on a power series decomposition of the covariance matrix, we describe the conditions under which very indirect interactions will have a pronounced effect on correlations and population dynamics. In random networks, we find that indirect interactions may lead to a broad distribution of activation levels with low average but highly variable correlations. This phenomenon is even more pronounced in networks with distance dependent connectivity. In contrast, networks with highly connected hubs or patchy connections often exhibit strong average correlations. Our results are particularly relevant in view of new experimental techniques that enable the parallel recording of spiking activity from a large number of neurons, an appropriate interpretation of which is hampered by the currently limited understanding of structure-dynamics relations in complex networks. Author Summary: Many biological systems have been described as networks whose complex properties influence the behaviour of the system. Correlations of activity in such networks are of interest in a variety of fields, from gene-regulatory networks to neuroscience. Due to novel experimental techniques allowing the recording of the activity of many pairs of neurons and their importance with respect to the functional interpretation of spike data, spike train correlations in neural networks have recently attracted a considerable amount of attention. Although origin and function of these correlations is not known in detail, they are believed to have a fundamental influence on information processing and learning. We present a detailed explanation of how recurrent connectivity induces correlations in local neural networks and how structural features affect their size and distribution. We examine under which conditions network characteristics like distance dependent connectivity, hubs or patches markedly influence correlations and population signals.

Suggested Citation

  • Volker Pernice & Benjamin Staude & Stefano Cardanobile & Stefan Rotter, 2011. "How Structure Determines Correlations in Neuronal Networks," PLOS Computational Biology, Public Library of Science, vol. 7(5), pages 1-14, May.
  • Handle: RePEc:plo:pcbi00:1002059
    DOI: 10.1371/journal.pcbi.1002059
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    Cited by:

    1. Gabriel Koch Ocker & Krešimir Josić & Eric Shea-Brown & Michael A Buice, 2017. "Linking structure and activity in nonlinear spiking networks," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-47, June.
    2. Stefano Recanatesi & Gabriel Koch Ocker & Michael A Buice & Eric Shea-Brown, 2019. "Dimensionality in recurrent spiking networks: Global trends in activity and local origins in connectivity," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-29, July.
    3. Richard Naud & Wulfram Gerstner, 2012. "Coding and Decoding with Adapting Neurons: A Population Approach to the Peri-Stimulus Time Histogram," PLOS Computational Biology, Public Library of Science, vol. 8(10), pages 1-14, October.
    4. Volker Pernice & Rava Azeredo da Silveira, 2018. "Interpretation of correlated neural variability from models of feed-forward and recurrent circuits," PLOS Computational Biology, Public Library of Science, vol. 14(2), pages 1-26, February.
    5. Andrea K Barreiro & Cheng Ly, 2017. "When do correlations increase with firing rates in recurrent networks?," PLOS Computational Biology, Public Library of Science, vol. 13(4), pages 1-30, April.
    6. Gabriel Koch Ocker & Ashok Litwin-Kumar & Brent Doiron, 2015. "Self-Organization of Microcircuits in Networks of Spiking Neurons with Plastic Synapses," PLOS Computational Biology, Public Library of Science, vol. 11(8), pages 1-40, August.
    7. Jonathan Schiefer & Alexander Niederbühl & Volker Pernice & Carolin Lennartz & Jürgen Hennig & Pierre LeVan & Stefan Rotter, 2018. "From correlation to causation: Estimating effective connectivity from zero-lag covariances of brain signals," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-18, March.
    8. Sadra Sadeh & Stefan Rotter, 2015. "Orientation Selectivity in Inhibition-Dominated Networks of Spiking Neurons: Effect of Single Neuron Properties and Network Dynamics," PLOS Computational Biology, Public Library of Science, vol. 11(1), pages 1-17, January.
    9. Tom Tetzlaff & Moritz Helias & Gaute T Einevoll & Markus Diesmann, 2012. "Decorrelation of Neural-Network Activity by Inhibitory Feedback," PLOS Computational Biology, Public Library of Science, vol. 8(8), pages 1-29, August.
    10. Chevallier, Julien & Ost, Guilherme, 2020. "Fluctuations for spatially extended Hawkes processes," Stochastic Processes and their Applications, Elsevier, vol. 130(9), pages 5510-5542.
    11. Naoki Masuda & Kazuyuki Aihara & Neil G. MacLaren, 2024. "Anticipating regime shifts by mixing early warning signals from different nodes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Sacha Jennifer van Albada & Moritz Helias & Markus Diesmann, 2015. "Scalability of Asynchronous Networks Is Limited by One-to-One Mapping between Effective Connectivity and Correlations," PLOS Computational Biology, Public Library of Science, vol. 11(9), pages 1-37, September.
    13. Means, Shawn & Laing, Carlo R., 2022. "Explosive behaviour in networks of Winfree oscillators," Chaos, Solitons & Fractals, Elsevier, vol. 160(C).
    14. James Trousdale & Yu Hu & Eric Shea-Brown & Krešimir Josić, 2012. "Impact of Network Structure and Cellular Response on Spike Time Correlations," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-15, March.
    15. Thibault Jaisson & Mathieu Rosenbaum, 2015. "Rough fractional diffusions as scaling limits of nearly unstable heavy tailed Hawkes processes," Papers 1504.03100, arXiv.org.
    16. Hualou Liang & Hongbin Wang, 2017. "Structure-Function Network Mapping and Its Assessment via Persistent Homology," PLOS Computational Biology, Public Library of Science, vol. 13(1), pages 1-19, January.
    17. Moritz Helias & Tom Tetzlaff & Markus Diesmann, 2014. "The Correlation Structure of Local Neuronal Networks Intrinsically Results from Recurrent Dynamics," PLOS Computational Biology, Public Library of Science, vol. 10(1), pages 1-21, January.
    18. Stojan Jovanović & Stefan Rotter, 2016. "Interplay between Graph Topology and Correlations of Third Order in Spiking Neuronal Networks," PLOS Computational Biology, Public Library of Science, vol. 12(6), pages 1-28, June.
    19. Pfaffelhuber, P. & Rotter, S. & Stiefel, J., 2022. "Mean-field limits for non-linear Hawkes processes with excitation and inhibition," Stochastic Processes and their Applications, Elsevier, vol. 153(C), pages 57-78.

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