Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep

By Bernhard P. Staresina, Til Ole Bergmann, Mathilde Bonnefond, Roemer van der Meij, Ole Jensen, Lorena Deuker, Christian Erich Elger, Nikolai Axmacher, J. Fell. 2015

749 citations recorded by the source corpus.

During systems-level consolidation, mnemonic representations initially reliant on the hippocampus are thought to migrate to neocortical sites for more permanent storage, with an eminent role of sleep for facilitating this information transfer. Mechanistically, consolidation processes have been hypothesized to rely on systematic interactions between the three cardinal neuronal oscillations characterizing non–rapid eye movement (NREM) sleep. Under global control of de- and hyperpolarizing slow oscillations (SOs), sleep spindles may cluster hippocampal ripples for a precisely timed transfer of local information to the neocortex. We used direct intracranial electroencephalogram recordings from human epilepsy patients during natural sleep to test the assumption that SOs, spindles and ripples are functionally coupled in the hippocampus. Employing cross-frequency phase-amplitude coupling analyses, we found that spindles were modulated by the up-state of SOs. Notably, spindles were found to in turn cluster ripples in their troughs, providing fine-tuned temporal frames for the hypothesized transfer of hippocampal memory traces.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “The nesting of ripples, spindles, and slow oscillations was reported in vivo (Staresina et al., 2015) and demonstrated in large-scale biophysical models (Sanda et al.”
An open-source, high-performance tool for automated sleep staging (2021, methodology): “…more complex and novel analysis methods that we and others have developed, including event-locked cross-frequency coupling ( Helfrich et al., 2018 ; Staresina et al., 2015 ) and decomposition of the sleep power spectrum into aperiodic and oscillatory components ( Lendner et al., 2020 ; Wen and…”
Post-learning hippocampal dynamics promote preferential retention of rewarding events (2016, positive): “In direct intracranial recordings from depth electrodes implanted in the human hippocampus, researchers have found evidence for SWR events during sleep (Staresina et al., 2015) and awake rest (Axmacher et al.”
Synaptic Mechanisms of Memory Consolidation during Sleep Slow Oscillations (2016, background): “, 2011), and spindles are temporally aligned with hippocampal ripples (Siapas and Wilson, 1998; Sirota et al., 2003; Staresina et al., 2015).”
Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep. (2020, neutral): “2017), and their nesting within hippocampus (Staresina et al. 2015).”
Echoes of Pink Noise: A Hypothesized Mechanism for Enhancing Sleep-Dependent Memory Consolidation with Auditory Stimulation (2025, unknown): “SOs provide a time window of opportunity for SW-Rs to occur, but they do not always spontaneously appear during these windows (Henin et al. 2019; Staresina et al. 2015).”
Widespread slow oscillations support interictal epileptiform discharge networks in focal epilepsy. (2024, background): “Phys-iologically, widespread SOs orchestrate brain activities by coordinating focal neuronal activities across distant regions (Skelin et al., 2021; Staresina et al., 2015).”
Neuronal oscillations in cognition: Down syndrome as a model of mouse to human translation (2024, unknown): “During periods of rest or sleep, hippocampal sharp-wave ripple (SWR) events are temporally coordinated with slow-wave oscillations across the cortex and have been proposed to be critical for memory consolidation (Rasch and Born 2013; Staresina and others 2015).”