IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1006643.html
   My bibliography  Save this article

Detection and analysis of spatiotemporal patterns in brain activity

Author

Listed:
  • Rory G Townsend
  • Pulin Gong

Abstract

There is growing evidence that population-level brain activity is often organized into propagating waves that are structured in both space and time. Such spatiotemporal patterns have been linked to brain function and observed across multiple recording methodologies and scales. The ability to detect and analyze these patterns is thus essential for understanding the working mechanisms of neural circuits. Here we present a mathematical and computational framework for the identification and analysis of multiple classes of wave patterns in neural population-level recordings. By drawing a conceptual link between spatiotemporal patterns found in the brain and coherent structures such as vortices found in turbulent flows, we introduce velocity vector fields to characterize neural population activity. These vector fields are calculated for both phase and amplitude of oscillatory neural signals by adapting optical flow estimation methods from the field of computer vision. Based on these velocity vector fields, we then introduce order parameters and critical point analysis to detect and characterize a diverse range of propagating wave patterns, including planar waves, sources, sinks, spiral waves, and saddle patterns. We also introduce a novel vector field decomposition method that extracts the dominant spatiotemporal structures in a recording. This enables neural data to be represented by the activity of a small number of independent spatiotemporal modes, providing an alternative to existing dimensionality reduction techniques which separate space and time components. We demonstrate the capabilities of the framework and toolbox with simulated data, local field potentials from marmoset visual cortex and optical voltage recordings from whole mouse cortex, and we show that pattern dynamics are non-random and are modulated by the presence of visual stimuli. These methods are implemented in a MATLAB toolbox, which is freely available under an open-source licensing agreement.Author summary: Structured activity such as propagating wave patterns at the level of neural circuits can arise from highly variable firing activity of individual neurons. This property makes the brain, a quintessential example of a complex system, analogous to other complex physical systems such as turbulent fluids, in which structured patterns like vortices similarly emerge from molecules that behave irregularly. In this study, by uniquely adapting techniques for the identification of coherent structures in fluid turbulence, we develop new analytical and computational methods for the reliable detection of a diverse range of propagating wave patterns in large-scale neural recordings, for comprehensive analysis and visualization of these patterns, and for analysis of their dominant spatiotemporal modes. We demonstrate that these methods can be used to uncover the essential spatiotemporal properties of neural population activity recorded by different modalities, thus offering new insights into understanding the working mechanisms of neural systems.

Suggested Citation

  • Rory G Townsend & Pulin Gong, 2018. "Detection and analysis of spatiotemporal patterns in brain activity," PLOS Computational Biology, Public Library of Science, vol. 14(12), pages 1-29, December.
  • Handle: RePEc:plo:pcbi00:1006643
    DOI: 10.1371/journal.pcbi.1006643
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1006643
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1006643&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1006643?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. Lyle Muller & Alexandre Reynaud & Frédéric Chavane & Alain Destexhe, 2014. "The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave," Nature Communications, Nature, vol. 5(1), pages 1-14, May.
    2. Alexander Thiele & Gene Stoner, 2003. "Neuronal synchrony does not correlate with motion coherence in cortical area MT," Nature, Nature, vol. 421(6921), pages 366-370, January.
    3. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Mondal, Argha & Hens, Chittaranjan & Mondal, Arnab & Antonopoulos, Chris G., 2021. "Spatiotemporal instabilities and pattern formation in systems of diffusively coupled Izhikevich neurons," Chaos, Solitons & Fractals, Elsevier, vol. 152(C).
    2. Yang Qi & Pulin Gong, 2022. "Fractional neural sampling as a theory of spatiotemporal probabilistic computations in neural circuits," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Yuqi Liang & Junhao Liang & Chenchen Song & Mianxin Liu & Thomas Knöpfel & Pulin Gong & Changsong Zhou, 2023. "Complexity of cortical wave patterns of the wake mouse cortex," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Fateev, I. & Polezhaev, A., 2024. "Chimera states in a lattice of superdiffusively coupled neurons," Chaos, Solitons & Fractals, Elsevier, vol. 181(C).
    5. Yifan Gu & Yang Qi & Pulin Gong, 2019. "Rich-club connectivity, diverse population coupling, and dynamical activity patterns emerging from local cortical circuits," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-34, April.
    6. Mondal, Arnab & Upadhyay, Ranjit Kumar & Mondal, Argha & Sharma, Sanjeev Kumar, 2022. "Emergence of Turing patterns and dynamic visualization in excitable neuron model," Applied Mathematics and Computation, Elsevier, vol. 423(C).

    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. Adeeti Aggarwal & Connor Brennan & Jennifer Luo & Helen Chung & Diego Contreras & Max B. Kelz & Alex Proekt, 2022. "Visual evoked feedforward–feedback traveling waves organize neural activity across the cortical hierarchy in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Joshua M. Diamond & Julio I. Chapeton & Weizhen Xie & Samantha N. Jackson & Sara K. Inati & Kareem A. Zaghloul, 2024. "Focal seizures induce spatiotemporally organized spiking activity in the human cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Jennifer B Tennessen & Marla M Holt & Brianna M Wright & M Bradley Hanson & Candice K Emmons & Deborah A Giles & Jeffrey T Hogan & Sheila J Thornton & Volker B Deecke, 2023. "Divergent foraging strategies between populations of sympatric matrilineal killer whales," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(3), pages 373-386.
    5. Thomas Schreiner & Marit Petzka & Tobias Staudigl & Bernhard P. Staresina, 2023. "Respiration modulates sleep oscillations and memory reactivation in humans," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    6. Andrew M. Clark & David C. Bradley, 2022. "A neural correlate of perceptual segmentation in macaque middle temporal cortical area," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Thomas Schreiner & Elisabeth Kaufmann & Soheyl Noachtar & Jan-Hinnerk Mehrkens & Tobias Staudigl, 2022. "The human thalamus orchestrates neocortical oscillations during NREM sleep," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Celia M. Gagliardi & Marc E. Normandin & Alexandra T. Keinath & Joshua B. Julian & Matthew R. Lopez & Manuel-Miguel Ramos-Alvarez & Russell A. Epstein & Isabel A. Muzzio, 2024. "Distinct neural mechanisms for heading retrieval and context recognition in the hippocampus during spatial reorientation," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    9. Dominik P. Koller & Michael Schirner & Petra Ritter, 2024. "Human connectome topology directs cortical traveling waves and shapes frequency gradients," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. Alireza Saeedi & Kun Wang & Ghazaleh Nikpourian & Andreas Bartels & Nikos K. Logothetis & Nelson K. Totah & Masataka Watanabe, 2024. "Brightness illusions drive a neuronal response in the primary visual cortex under top-down modulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Arthur Pewsey & Eduardo García-Portugués, 2021. "Recent advances in directional statistics," TEST: An Official Journal of the Spanish Society of Statistics and Operations Research, Springer;Sociedad de Estadística e Investigación Operativa, vol. 30(1), pages 1-58, March.
    12. Thomas Schreiner & Benjamin J. Griffiths & Merve Kutlu & Christian Vollmar & Elisabeth Kaufmann & Stefanie Quach & Jan Remi & Soheyl Noachtar & Tobias Staudigl, 2024. "Spindle-locked ripples mediate memory reactivation during human NREM sleep," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. César Henrique Mattos Pires & Felipe M. Pimenta & Carla A. D'Aquino & Osvaldo R. Saavedra & Xuerui Mao & Arcilan T. Assireu, 2020. "Coastal Wind Power in Southern Santa Catarina, Brazil," Energies, MDPI, vol. 13(19), pages 1-23, October.
    14. Alexis T Baria & Brian Maniscalco & Biyu J He, 2017. "Initial-state-dependent, robust, transient neural dynamics encode conscious visual perception," PLOS Computational Biology, Public Library of Science, vol. 13(11), pages 1-29, November.
    15. Matthijs J. Warrens & Bunga C. Pratiwi, 2016. "Kappa Coefficients for Circular Classifications," Journal of Classification, Springer;The Classification Society, vol. 33(3), pages 507-522, October.
    16. James Rankin & Frédéric Chavane, 2017. "Neural field model to reconcile structure with function in primary visual cortex," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-30, October.
    17. Lombard, F. & Hawkins, Douglas M. & Potgieter, Cornelis J., 2017. "Sequential rank CUSUM charts for angular data," Computational Statistics & Data Analysis, Elsevier, vol. 105(C), pages 268-279.
    18. Masataka Sawayama & Shin'ya Nishida, 2018. "Material and shape perception based on two types of intensity gradient information," PLOS Computational Biology, Public Library of Science, vol. 14(4), pages 1-40, April.
    19. Aguiar-Conraria, Luis & Martins, Manuel M.F. & Soares, Maria Joana, 2018. "Estimating the Taylor rule in the time-frequency domain," Journal of Macroeconomics, Elsevier, vol. 57(C), pages 122-137.
    20. Assaf Breska & Leon Y Deouell, 2017. "Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment," PLOS Biology, Public Library of Science, vol. 15(2), pages 1-30, February.

    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:pcbi00:1006643. 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: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    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.