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Population burst propagation across interacting areas of the brain

For many perceptual and behavioral tasks, a prominent feature of neural spike trains involves high firing rates across relatively short intervals of time. We call these events “population bursts.” Because during a population burst information is, presumably, transmitted from one part of the brain to...

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Autores principales: Chen, Yu, Douglas, Hannah, Medina, Bryan J., Olarinre, Motolani, Siegle, Joshua H., Kass, Robert E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744659/
https://www.ncbi.nlm.nih.gov/pubmed/36321709
http://dx.doi.org/10.1152/jn.00066.2022
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author Chen, Yu
Douglas, Hannah
Medina, Bryan J.
Olarinre, Motolani
Siegle, Joshua H.
Kass, Robert E.
author_facet Chen, Yu
Douglas, Hannah
Medina, Bryan J.
Olarinre, Motolani
Siegle, Joshua H.
Kass, Robert E.
author_sort Chen, Yu
collection PubMed
description For many perceptual and behavioral tasks, a prominent feature of neural spike trains involves high firing rates across relatively short intervals of time. We call these events “population bursts.” Because during a population burst information is, presumably, transmitted from one part of the brain to another, burst timing should reveal activity related to the flow of information across neural circuits. We developed a statistical method (based on a point process model) of determining, accurately, the time of the maximum (peak) population firing rate on a trial-by-trial basis and used it to characterize burst propagation across areas. We then examined the tendency of peak firing rates in distinct brain areas to shift earlier or later in time, together, across repeated trials, and found this trial-to-trial coupling of peak times to be a sensitive indicator of interaction across populations. In the data we examined, from the Allen Brain Observatory, we found many very strong correlations (95% confidence intervals above 0.75) in cases where standard methods were unable to demonstrate cross-area correlation. The statistical model introduced cross-area covariation only through population-level trial-dependent time shifts and gain constants (values of which were learned from the data), yet it provided very good fits to data histograms, including histograms of spike count correlations within and across visual areas. Our results demonstrate the utility of carefully assessing timing and propagation, across brain regions, of transient bursts in neural population activity, based on multiple spike train recordings. NEW & NOTEWORTHY We developed a novel statistical method for identifying coordinated propagation of activity across populations of spiking neurons, with high temporal accuracy. Using simultaneous recordings from three visual areas we document precise timing relationships on a trial-by-trial basis, and we show how previously existing techniques can fail to discover coordinated activity in cases where the new approach finds very strong cross-area correlation.
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spelling pubmed-97446592023-01-17 Population burst propagation across interacting areas of the brain Chen, Yu Douglas, Hannah Medina, Bryan J. Olarinre, Motolani Siegle, Joshua H. Kass, Robert E. J Neurophysiol Innovative Methodology For many perceptual and behavioral tasks, a prominent feature of neural spike trains involves high firing rates across relatively short intervals of time. We call these events “population bursts.” Because during a population burst information is, presumably, transmitted from one part of the brain to another, burst timing should reveal activity related to the flow of information across neural circuits. We developed a statistical method (based on a point process model) of determining, accurately, the time of the maximum (peak) population firing rate on a trial-by-trial basis and used it to characterize burst propagation across areas. We then examined the tendency of peak firing rates in distinct brain areas to shift earlier or later in time, together, across repeated trials, and found this trial-to-trial coupling of peak times to be a sensitive indicator of interaction across populations. In the data we examined, from the Allen Brain Observatory, we found many very strong correlations (95% confidence intervals above 0.75) in cases where standard methods were unable to demonstrate cross-area correlation. The statistical model introduced cross-area covariation only through population-level trial-dependent time shifts and gain constants (values of which were learned from the data), yet it provided very good fits to data histograms, including histograms of spike count correlations within and across visual areas. Our results demonstrate the utility of carefully assessing timing and propagation, across brain regions, of transient bursts in neural population activity, based on multiple spike train recordings. NEW & NOTEWORTHY We developed a novel statistical method for identifying coordinated propagation of activity across populations of spiking neurons, with high temporal accuracy. Using simultaneous recordings from three visual areas we document precise timing relationships on a trial-by-trial basis, and we show how previously existing techniques can fail to discover coordinated activity in cases where the new approach finds very strong cross-area correlation. American Physiological Society 2022-12-01 2022-11-02 /pmc/articles/PMC9744659/ /pubmed/36321709 http://dx.doi.org/10.1152/jn.00066.2022 Text en Copyright © 2022 The Authors https://creativecommons.org/licenses/by/4.0/Licensed under Creative Commons Attribution CC-BY 4.0 (https://creativecommons.org/licenses/by/4.0/) . Published by the American Physiological Society.
spellingShingle Innovative Methodology
Chen, Yu
Douglas, Hannah
Medina, Bryan J.
Olarinre, Motolani
Siegle, Joshua H.
Kass, Robert E.
Population burst propagation across interacting areas of the brain
title Population burst propagation across interacting areas of the brain
title_full Population burst propagation across interacting areas of the brain
title_fullStr Population burst propagation across interacting areas of the brain
title_full_unstemmed Population burst propagation across interacting areas of the brain
title_short Population burst propagation across interacting areas of the brain
title_sort population burst propagation across interacting areas of the brain
topic Innovative Methodology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9744659/
https://www.ncbi.nlm.nih.gov/pubmed/36321709
http://dx.doi.org/10.1152/jn.00066.2022
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