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An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep

View ORCID ProfileFrank J. van Schalkwijk, View ORCID ProfileJan Weber, View ORCID ProfileMichael A. Hahn, View ORCID ProfileJanna D. Lendner, Marion Inostroza, View ORCID ProfileJack J. Lin, View ORCID ProfileRandolph F. Helfrich
doi: https://doi.org/10.1101/2022.10.19.512822
Frank J. van Schalkwijk
1Hertie-Institute for Clinical Brain Research, Center for Neurology, University Medical Center Tübingen, Otfried-Müller Str. 27, 72076 Tübingen, Germany
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  • For correspondence: randolph.helfrich@gmail.com
Jan Weber
1Hertie-Institute for Clinical Brain Research, Center for Neurology, University Medical Center Tübingen, Otfried-Müller Str. 27, 72076 Tübingen, Germany
2International Max Planck Research School for the Mechanisms of Mental Function and Dysfunction, University of Tübingen, Germany
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Michael A. Hahn
1Hertie-Institute for Clinical Brain Research, Center for Neurology, University Medical Center Tübingen, Otfried-Müller Str. 27, 72076 Tübingen, Germany
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Janna D. Lendner
1Hertie-Institute for Clinical Brain Research, Center for Neurology, University Medical Center Tübingen, Otfried-Müller Str. 27, 72076 Tübingen, Germany
3Department of Anesthesiology and Intensive Care Medicine, University Medical Center Tübingen; Hoppe-Seyler-Str 3, 72076 Tübingen, Germany
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Marion Inostroza
4Institute of Medical Psychology and Behavioral Neurobiology, University of Tübingen, Tübingen, Germany
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Jack J. Lin
5Department of Neurology, University of California, Davis, 4860 Y St., Sacramento, CA 95817, USA
6The Center for Mind and Brain, University of California, Davis, Davis, CA 95618, USA
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Randolph F. Helfrich
1Hertie-Institute for Clinical Brain Research, Center for Neurology, University Medical Center Tübingen, Otfried-Müller Str. 27, 72076 Tübingen, Germany
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  • For correspondence: randolph.helfrich@gmail.com
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Abstract

The hippocampal sharp-wave ripple (SW-R) is the key substrate of the hippocampal-neocortical dialogue underlying memory formation. Recently, it became evident that SW-R are not unique to archicortex, but constitute a wide-spread neocortical phenomenon. To date, little is known about morphological and functional similarities between archi- and neocortical SW-R. Leveraging intracranial recordings from the human hippocampus and prefrontal cortex during sleep, our results reveal region-specific functional specializations, albeit a near-uniform morphology. While hippocampal SW-R trigger directional hippocampal-to-neocortical information flow, neocortical SW-R reduce information flow to minimize interference. At the population level, hippocampal SW-R confined population dynamics to a low-dimensional subspace, while neocortical SW-R diversified the population response; functionally uncoupling the hippocampal-neocortical network. Critically, our replication in rodents demonstrated the same division-of-labor between archi-and neocortical SW-R. These results uncover an evolutionary preserved mechanism where coordinated interplay between hippocampal and neocortical SW-R temporally segregates hippocampal information transfer from neocortical processing.

Competing Interest Statement

The authors have declared no competing interest.

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Posted October 21, 2022.
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An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep
Frank J. van Schalkwijk, Jan Weber, Michael A. Hahn, Janna D. Lendner, Marion Inostroza, Jack J. Lin, Randolph F. Helfrich
bioRxiv 2022.10.19.512822; doi: https://doi.org/10.1101/2022.10.19.512822
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An evolutionary conserved division-of-labor between hippocampal and neocortical sharp-wave ripples organizes information transfer during sleep
Frank J. van Schalkwijk, Jan Weber, Michael A. Hahn, Janna D. Lendner, Marion Inostroza, Jack J. Lin, Randolph F. Helfrich
bioRxiv 2022.10.19.512822; doi: https://doi.org/10.1101/2022.10.19.512822

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