Human REM sleep recalibrates neural activity in support of memory formation

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.

Authors:

• Janna D. Lendner

• Niels Niethard

• Bryce A. Mander

• Frank J. van Schalkwijk

• Sigrid Schuh-Hofer

• Hannah Schmidt

• Robert T. Knight

• Jan Born

• Matthew P. Walker

• Jack J. Lin

• Randolph F. Helfrich

Date: 2023

DOI: DOI: 10.1126/sciadv.adj1895

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Human in vivo tau pathology, impaired NREM sleep oscillations and memory decline in aging

Abstract:

Aging disrupts sleep. Moreover, these sleep impairments are exaggerated in Alzheimer’s disease, and are proposed to contribute to cognitive decline. Recent human studies have linked β-amyloid with non-rapid eye-movement (NREM) sleep disruption. However, the impact of tau pathology on human sleep oscillations and cognition remains uninvestigated. Here, we tested the hypothesis that tau burden within medial temporal lobe (MTL) impairs the coupled relationship between the two key NREM sleep oscillations—sleep spindles and slow waves, and their known support of hippocampal memory.

Authors:

• Joseph R. Winer

• Bryce A. Mander

• Randolph F. Helfrich

• Anne Maass

• Theresa M. Harrison

• Suzanne L. Baker

• Robert T. Knight

• William J. Jagust

• Matthew P. Walker

Date: 2018

DOI: 10.1016/j.jalz.2018.06.2344

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Multiplexing of Theta and Alpha Rhythms in the Amygdala-Hippocampal Circuit Supports Pattern Separation of Emotional Information

ABSTRACT

How do we remember emotional events? While emotion often leads to vivid recollection, the precision of emotional memories can be degraded, especially when discriminating among overlapping experiences in memory (i.e. pattern separation). Communication between the amygdala and the hippocampus has been proposed to support emotional memory but the exact neural mechanisms are not well understood. Here, we used intracranial depth electrode recordings in pre-surgical epilepsy patients to show that successful pattern separation of emotional stimuli is associated with theta band (3-7 Hz)-coordinated bidirectional interactions between the amygdala and the hippocampus. In contrast, we show that overgeneralization is associated with alpha band (7-13 Hz)-coordinated unidirectional influence from the amygdala to the hippocampus. These findings imply that alpha band synchrony may trigger overgeneralization of similar emotional events via amygdala-hippocampal directional coupling, which suggests a target for the treatment of psychiatric conditions such as post-traumatic stress disorder, where aversive memories are often overgeneralized.

AUTHORS

• Jie Zheng

• Rebecca F. Stevenson

• Bryce A. Mander

• Lilit Mnatsakanyan

• Frank P. K. Hsu

• Sumeet Vadera

• Robert T. Knight

• Michael A. Yassa

• Jack J. Lin

Date: 2018

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Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting

ABSTRACT

The coupled interaction between slow-wave oscillations and sleep spindles during non-rapid-eye-movement (NREM) sleep has been proposed to support memory consolidation. However, little evidence in humans supports this theory. Moreover, whether such dynamic coupling is impaired as a consequence of brain aging in later life, contributing to cognitive and memory decline, is unknown. Combining electroencephalography (EEG), structural MRI, and sleep-dependent memory assessment, we addressed these questions in cognitively normal young and older adults. Directional cross-frequency coupling analyses demonstrated that the slow wave governs a precise temporal coordination of sleep spindles, the quality of which predicts overnight memory retention. Moreover, selective atrophy within the medial frontal cortex in older adults predicted a temporal dispersion of this slow wave-spindle coupling, impairing overnight memory consolidation and leading to forgetting. Prefrontal-dependent deficits in the spatiotemporal coordination of NREM sleep oscillations therefore represent one pathway explaining age-related memory decline.

AUTHORS

• Randolph F. Helfrich

• Bryce A. Mander

• William J. Jagust

• Robert T. Knight

• Matthew P. Walker

Date: 2018

DOI: 10.1016/j.neuron.2017.11.020

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