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Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans

Synchronous bursts of high frequency oscillations (‘ripples’) are hypothesized to contribute to binding by facilitating integration of neuronal firing across cortical locations. We tested this hypothesis using local field-potentials and single-unit firing from four 96-channel microelectrode arrays i...

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Autores principales: Verzhbinsky, Ilya A., Rubin, Daniel B., Kajfez, Sophie, Bu, Yiting, Kelemen, Jessica N., Kapitonava, Anastasia, Williams, Ziv M., Hochberg, Leigh R., Cash, Sydney S., Halgren, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245779/
https://www.ncbi.nlm.nih.gov/pubmed/37292943
http://dx.doi.org/10.1101/2023.05.20.541588
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author Verzhbinsky, Ilya A.
Rubin, Daniel B.
Kajfez, Sophie
Bu, Yiting
Kelemen, Jessica N.
Kapitonava, Anastasia
Williams, Ziv M.
Hochberg, Leigh R.
Cash, Sydney S.
Halgren, Eric
author_facet Verzhbinsky, Ilya A.
Rubin, Daniel B.
Kajfez, Sophie
Bu, Yiting
Kelemen, Jessica N.
Kapitonava, Anastasia
Williams, Ziv M.
Hochberg, Leigh R.
Cash, Sydney S.
Halgren, Eric
author_sort Verzhbinsky, Ilya A.
collection PubMed
description Synchronous bursts of high frequency oscillations (‘ripples’) are hypothesized to contribute to binding by facilitating integration of neuronal firing across cortical locations. We tested this hypothesis using local field-potentials and single-unit firing from four 96-channel microelectrode arrays in supragranular cortex of 3 patients. Neurons in co-rippling locations showed increased short-latency co-firing, prediction of each-other’s firing, and co-participation in neural assemblies. Effects were similar for putative pyramidal and interneurons, during NREM sleep and waking, in temporal and Rolandic cortices, and at distances up to 16mm. Increased co-prediction during co-ripples was maintained when firing-rate changes were equated, and were strongly modulated by ripple phase. Co-ripple enhanced prediction is reciprocal, synergistic with local upstates, and further enhanced when multiple sites co-ripple. Together, these results support the hypothesis that trans-cortical co-ripples increase the integration of neuronal firing of neurons in different cortical locations, and do so in part through phase-modulation rather than unstructured activation.
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spelling pubmed-102457792023-06-08 Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans Verzhbinsky, Ilya A. Rubin, Daniel B. Kajfez, Sophie Bu, Yiting Kelemen, Jessica N. Kapitonava, Anastasia Williams, Ziv M. Hochberg, Leigh R. Cash, Sydney S. Halgren, Eric bioRxiv Article Synchronous bursts of high frequency oscillations (‘ripples’) are hypothesized to contribute to binding by facilitating integration of neuronal firing across cortical locations. We tested this hypothesis using local field-potentials and single-unit firing from four 96-channel microelectrode arrays in supragranular cortex of 3 patients. Neurons in co-rippling locations showed increased short-latency co-firing, prediction of each-other’s firing, and co-participation in neural assemblies. Effects were similar for putative pyramidal and interneurons, during NREM sleep and waking, in temporal and Rolandic cortices, and at distances up to 16mm. Increased co-prediction during co-ripples was maintained when firing-rate changes were equated, and were strongly modulated by ripple phase. Co-ripple enhanced prediction is reciprocal, synergistic with local upstates, and further enhanced when multiple sites co-ripple. Together, these results support the hypothesis that trans-cortical co-ripples increase the integration of neuronal firing of neurons in different cortical locations, and do so in part through phase-modulation rather than unstructured activation. Cold Spring Harbor Laboratory 2023-06-13 /pmc/articles/PMC10245779/ /pubmed/37292943 http://dx.doi.org/10.1101/2023.05.20.541588 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Verzhbinsky, Ilya A.
Rubin, Daniel B.
Kajfez, Sophie
Bu, Yiting
Kelemen, Jessica N.
Kapitonava, Anastasia
Williams, Ziv M.
Hochberg, Leigh R.
Cash, Sydney S.
Halgren, Eric
Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans
title Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans
title_full Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans
title_fullStr Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans
title_full_unstemmed Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans
title_short Co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans
title_sort co-occurring ripple oscillations facilitate neuronal interactions between cortical locations in humans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245779/
https://www.ncbi.nlm.nih.gov/pubmed/37292943
http://dx.doi.org/10.1101/2023.05.20.541588
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