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.Research output: Contribution to journal › Article › peer-review
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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 -