Human REM sleep recalibrates neural activity in support of memory formation

Author:

Lendner Janna D.12ORCID,Niethard Niels3ORCID,Mander Bryce A.4,van Schalkwijk Frank J.1ORCID,Schuh-Hofer Sigrid56,Schmidt Hannah5ORCID,Knight Robert T.78ORCID,Born Jan3910ORCID,Walker Matthew P.78,Lin Jack J.1112,Helfrich Randolph F.16ORCID

Affiliation:

1. Hertie Institute for Clinical Brain Research, Center for Neurology, University Medical Center Tübingen, Hoppe-Seyler-Str 3, 72076 Tübingen, Germany.

2. Department of Anesthesiology and Intensive Care Medicine, University Medical Center Tübingen, Hoppe-Seyler-Str 3, 72076 Tübingen, Germany.

3. Institute of Medical Psychology and Behavioral Neurobiology, University of Tübingen, Tübingen 72076, Germany.

4. Department of Psychiatry and Human Behavior, UC Irvine, 101 The City Dr, Orange, CA 92868, USA.

5. Department of Neurophysiology, University Medical Center Mannheim, Ludolf-Krehl-Str. 13-17, 68167 Mannheim, Germany.

6. Department of Neurology and Epileptology, University Medical Center Tübingen, Hoppe-Seyler-Str 3, 72076 Tübingen, Germany.

7. Helen Wills Neuroscience Institute, UC Berkeley, 130 Barker Hall, CA 94720, USA.

8. Department of Psychology, UC Berkeley, 2121 Berkeley Way, CA 94720, USA.

9. Center for Integrative Neuroscience, University of Tübingen, Tübingen 72076, Germany.

10. German Center for Diabetes Research (DZD), Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen (IDM), Tübingen 72076, Germany.

11. Department of Neurology, UC Davis, 3160 Folsom Blvd., Sacramento, CA 95816, USA.

12. Center for Mind and Brain, UC Davis, 267 Cousteau Pl, Davis, CA 95618, USA.

Abstract

The proposed mechanisms of sleep-dependent memory consolidation involve the overnight regulation of neural activity at both synaptic and whole-network levels. Now, there is a lack of in vivo data in humans elucidating if, and how, sleep and its varied stages balance neural activity, and if such recalibration benefits memory. We combined electrophysiology with in vivo two-photon calcium imaging in rodents as well as intracranial and scalp electroencephalography (EEG) in humans to reveal a key role for non-oscillatory brain activity during rapid eye movement (REM) sleep to mediate sleep-dependent recalibration of neural population dynamics. The extent of this REM sleep recalibration predicted the success of overnight memory consolidation, expressly the modulation of hippocampal—neocortical activity, favoring remembering rather than forgetting. The findings describe a non-oscillatory mechanism how human REM sleep modulates neural population activity to enhance long-term memory.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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