Literature DB >> 34001599

Coupling between slow waves and sharp-wave ripples engages distributed neural activity during sleep in humans.

Ivan Skelin1,2, Haoxin Zhang3,4, Jie Zheng4, Shiting Ma3, Bryce A Mander5, Olivia Kim McManus6,7, Sumeet Vadera8, Robert T Knight9,10, Bruce L McNaughton2,11, Jack J Lin1,4.   

Abstract

Hippocampal-dependent memory consolidation during sleep is hypothesized to depend on the synchronization of distributed neuronal ensembles, organized by the hippocampal sharp-wave ripples (SWRs, 80 to 150 Hz), subcortical/cortical slow-wave activity (SWA, 0.5 to 4 Hz), and sleep spindles (SP, 7 to 15 Hz). However, the precise role of these interactions in synchronizing subcortical/cortical neuronal activity is unclear. Here, we leverage intracranial electrophysiological recordings from the human hippocampus, amygdala, and temporal and frontal cortices to examine activity modulation and cross-regional coordination during SWRs. Hippocampal SWRs are associated with widespread modulation of high-frequency activity (HFA, 70 to 200 Hz), a measure of local neuronal activation. This peri-SWR HFA modulation is predicted by the coupling between hippocampal SWRs and local subcortical/cortical SWA or SP. Finally, local cortical SWA phase offsets and SWR amplitudes predicted functional connectivity between the frontal and temporal cortex during individual SWRs. These findings suggest a selection mechanism wherein hippocampal SWR and cortical slow-wave synchronization governs the transient engagement of distributed neuronal populations supporting hippocampal-dependent memory consolidation.

Entities:  

Keywords:  human brain; sharp wave/ripples; sleep; slow waves; spindles

Mesh:

Year:  2021        PMID: 34001599      PMCID: PMC8166184          DOI: 10.1073/pnas.2012075118

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  53 in total

1.  Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics.

Authors:  H S Kudrimoti; C A Barnes; B L McNaughton
Journal:  J Neurosci       Date:  1999-05-15       Impact factor: 6.167

2.  Modulation of neuronal interactions through neuronal synchronization.

Authors:  Thilo Womelsdorf; Jan-Mathijs Schoffelen; Robert Oostenveld; Wolf Singer; Robert Desimone; Andreas K Engel; Pascal Fries
Journal:  Science       Date:  2007-06-15       Impact factor: 47.728

3.  Source modeling sleep slow waves.

Authors:  Michael Murphy; Brady A Riedner; Reto Huber; Marcello Massimini; Fabio Ferrarelli; Giulio Tononi
Journal:  Proc Natl Acad Sci U S A       Date:  2009-01-22       Impact factor: 11.205

4.  Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep.

Authors:  A G Siapas; M A Wilson
Journal:  Neuron       Date:  1998-11       Impact factor: 17.173

5.  Hippocampo-cortical coupling mediates memory consolidation during sleep.

Authors:  Nicolas Maingret; Gabrielle Girardeau; Ralitsa Todorova; Marie Goutierre; Michaël Zugaro
Journal:  Nat Neurosci       Date:  2016-05-16       Impact factor: 24.884

6.  The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks.

Authors:  M Steriade; D Contreras; R Curró Dossi; A Nuñez
Journal:  J Neurosci       Date:  1993-08       Impact factor: 6.167

7.  Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans.

Authors:  Jeremy R Manning; Joshua Jacobs; Itzhak Fried; Michael J Kahana
Journal:  J Neurosci       Date:  2009-10-28       Impact factor: 6.167

8.  Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans.

Authors:  Zsófia Clemens; Matthias Mölle; Lóránd Eross; Péter Barsi; Péter Halász; Jan Born
Journal:  Brain       Date:  2007-07-05       Impact factor: 13.501

9.  Cell type-specific firing during ripple oscillations in the hippocampal formation of humans.

Authors:  Michel Le Van Quyen; Anatol Bragin; Richard Staba; Benoit Crépon; Charles L Wilson; Jerome Engel
Journal:  J Neurosci       Date:  2008-06-11       Impact factor: 6.167

10.  Integrated analysis of anatomical and electrophysiological human intracranial data.

Authors:  Arjen Stolk; Sandon Griffin; Roemer van der Meij; Callum Dewar; Ignacio Saez; Jack J Lin; Giovanni Piantoni; Jan-Mathijs Schoffelen; Robert T Knight; Robert Oostenveld
Journal:  Nat Protoc       Date:  2018-07       Impact factor: 13.491

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Review 2.  Brain neural patterns and the memory function of sleep.

Authors:  Gabrielle Girardeau; Vítor Lopes-Dos-Santos
Journal:  Science       Date:  2021-10-28       Impact factor: 47.728

Review 3.  Long-Range GABAergic Projections of Cortical Origin in Brain Function.

Authors:  Jocelyn Urrutia-Piñones; Camila Morales-Moraga; Nicole Sanguinetti-González; Angelica P Escobar; Chiayu Q Chiu
Journal:  Front Syst Neurosci       Date:  2022-03-22

4.  Advanced age has dissociable effects on hippocampal CA1 ripples and CA3 high frequency events in male rats.

Authors:  Nicholas M DiCola; Alexa L Lacy; Omar J Bishr; Kathryn M Kimsey; Jenna L Whitney; Sarah D Lovett; Sara N Burke; Andrew P Maurer
Journal:  Neurobiol Aging       Date:  2022-05-05       Impact factor: 5.133

  4 in total

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