Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples

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Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples. / Ngo, Hong Viet; Fell, Juergen; Staresina, Bernhard.

In: Elife, Vol. 9, e57011, 13.07.2020, p. 1-18.

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@article{e279d82e7bc649d883f1f56151f01228,
title = "Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples",
abstract = "Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.",
keywords = "hippocampus, human, neuroscience, ripples, sleep, spindles",
author = "Ngo, {Hong Viet} and Juergen Fell and Bernhard Staresina",
note = "{\textcopyright} 2020, Ngo et al.",
year = "2020",
month = jul,
day = "13",
doi = "10.7554/eLife.57011",
language = "English",
volume = "9",
pages = "1--18",
journal = "Elife",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

}

RIS

TY - JOUR

T1 - Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples

AU - Ngo, Hong Viet

AU - Fell, Juergen

AU - Staresina, Bernhard

N1 - © 2020, Ngo et al.

PY - 2020/7/13

Y1 - 2020/7/13

N2 - Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.

AB - Sleep is pivotal for memory consolidation. According to two-stage accounts, memory traces are gradually translocated from hippocampus to neocortex during non-rapid-eye-movement (NREM) sleep. Mechanistically, this information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. To test this hypothesis, we analyzed intracranial and scalp Electroencephalography sleep recordings from pre-surgical epilepsy patients. We first observed a concurrent spindle power increase in hippocampus (HIPP) and neocortex (NC) time-locked to individual hippocampal ripple events. Coherence analysis confirmed elevated levels of hippocampal-neocortical spindle coupling around ripples, with directionality analyses indicating an influence from NC to HIPP. Importantly, these hippocampal-neocortical dynamics were particularly pronounced during long-duration compared to short-duration ripples. Together, our findings reveal a potential mechanism underlying active consolidation, comprising a neocortical-hippocampal-neocortical reactivation loop initiated by the neocortex. This hippocampal-cortical dialogue is mediated by sleep spindles and is enhanced during long-duration hippocampal ripples.

KW - hippocampus

KW - human

KW - neuroscience

KW - ripples

KW - sleep

KW - spindles

UR - http://www.scopus.com/inward/record.url?scp=85088253434&partnerID=8YFLogxK

U2 - 10.7554/eLife.57011

DO - 10.7554/eLife.57011

M3 - Article

C2 - 32657268

AN - SCOPUS:85088253434

VL - 9

SP - 1

EP - 18

JO - Elife

JF - Elife

SN - 2050-084X

M1 - e57011

ER -