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Detection and analysis of spatiotemporal patterns in brain activity

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  • 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
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    References listed on IDEAS

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    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).
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    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. 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.
    3. 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.
    4. 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.
    5. 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).

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