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Replay of large-scale spatio-temporal patterns from waking during subsequent slow-wave sleep in human cortex

Xi Jiang, Isaac Shamie, Werner Doyle, Daniel Friedman, Patricia Dugan, Orrin Devinsky, Emad Eskandar, Sydney S. Cash, Thomas Thesen, Eric Halgren
doi: https://doi.org/10.1101/221275
Xi Jiang
1Neurosciences Graduate Program, University of California at San Diego, La Jolla, CA 92093, USA.
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  • For correspondence: x4jiang@ucsd.edu ehalgren@ucsd.edu
Isaac Shamie
1aDepartment of Radiology, University of California at San Diego, La Jolla, CA 92093, USA.
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Werner Doyle
2Comprehensive Epilepsy Center, New York University School of Medicine, New York, NY 10016, USA.
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Daniel Friedman
2Comprehensive Epilepsy Center, New York University School of Medicine, New York, NY 10016, USA.
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Patricia Dugan
2Comprehensive Epilepsy Center, New York University School of Medicine, New York, NY 10016, USA.
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Orrin Devinsky
2Comprehensive Epilepsy Center, New York University School of Medicine, New York, NY 10016, USA.
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Emad Eskandar
3Department of Neurosurgery, Epilepsy Division, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
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Sydney S. Cash
4Department of Neurology, Epilepsy Division, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
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Thomas Thesen
2Comprehensive Epilepsy Center, New York University School of Medicine, New York, NY 10016, USA.
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Eric Halgren
1aDepartment of Radiology, University of California at San Diego, La Jolla, CA 92093, USA.
5Department of Neurosciences, University of California at San Diego, La Jolla, CA 92093, USA.
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  • For correspondence: x4jiang@ucsd.edu ehalgren@ucsd.edu
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Abstract

Animal studies support the hypothesis that in slow-wave sleep, replay of waking neocortical activity under hippocampal guidance leads to memory consolidation. However, no intracranial electrophysiological evidence for replay exists in humans. We identified consistent sequences of population firing peaks across widespread cortical regions during complete waking periods. The occurrence of these Motifs were compared between sleeps preceding the waking period (Sleep-Pre) when the Motifs were identified, and those following (Sleep-Post). In all subjects, the majority of waking Motifs (most of which were novel) had more matches in Sleep-Post than in Sleep-Pre. In rodents, hippocampal replay occurs during local sharp-wave ripples, and the associated neocortical replay tends to occur during local sleep spindles and down-to-up transitions. These waves may facilitate consolidation by sequencing cell-firing and encouraging plasticity. Similarly, we found that Motifs were coupled to neocortical spindles, down-to-up transitions, theta bursts, and hippocampal sharp-wave ripples. While Motifs occurring during cognitive task performance were more likely to have more matches in subsequent sleep, our studies provide no direct demonstration that the replay of Motifs contributes to consolidation. Nonetheless, these results confirm a core prediction of the dominant neurobiological theory of human memory consolidation.

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Posted November 17, 2017.
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Replay of large-scale spatio-temporal patterns from waking during subsequent slow-wave sleep in human cortex
Xi Jiang, Isaac Shamie, Werner Doyle, Daniel Friedman, Patricia Dugan, Orrin Devinsky, Emad Eskandar, Sydney S. Cash, Thomas Thesen, Eric Halgren
bioRxiv 221275; doi: https://doi.org/10.1101/221275
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Replay of large-scale spatio-temporal patterns from waking during subsequent slow-wave sleep in human cortex
Xi Jiang, Isaac Shamie, Werner Doyle, Daniel Friedman, Patricia Dugan, Orrin Devinsky, Emad Eskandar, Sydney S. Cash, Thomas Thesen, Eric Halgren
bioRxiv 221275; doi: https://doi.org/10.1101/221275

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