TY - JOUR
T1 - Thalamic Spindles Promote Memory Formation during Sleep through Triple Phase-Locking of Cortical, Thalamic, and Hippocampal Rhythms
AU - Latchoumane, Charles Francois V.
AU - Ngo, Hong Viet V.
AU - Born, Jan
AU - Shin, Hee Sup
N1 - Funding Information:
This work was supported by the grant IBS-R001-D1 from the Institute for Basic Science, Korea, the Deutsche Forschungsgemeinschaft (Tr-SFB 654 ?Plasticity and Sleep?), and the German Federal Ministry of Education and Research (01GI0925 and 01GQ0973). We thank Matthias M?lle, Eunyoung Bang, Boyoung Lee, Yooncheol Jang, Joon-Hyuk Lee, and Seung-eun Lee for experimental support.
Funding Information:
This work was supported by the grant IBS-R001-D1 from the Institute for Basic Science , Korea, the Deutsche Forschungsgemeinschaft ( Tr-SFB 654 “Plasticity and Sleep”), and the German Federal Ministry of Education and Research ( 01GI0925 and 01GQ0973 ). We thank Matthias Mölle, Eunyoung Bang, Boyoung Lee, Yooncheol Jang, Joon-Hyuk Lee, and Seung-eun Lee for experimental support.
Publisher Copyright:
© 2017 Elsevier Inc.
Copyright:
Copyright 2017 Elsevier B.V., All rights reserved.
PY - 2017/7/19
Y1 - 2017/7/19
N2 - While the interaction of the cardinal rhythms of non-rapid-eye-movement (NREM) sleep—the thalamo-cortical spindles, hippocampal ripples, and the cortical slow oscillations—is thought to be critical for memory consolidation during sleep, the role spindles play in this interaction is elusive. Combining optogenetics with a closed-loop stimulation approach in mice, we show here that only thalamic spindles induced in-phase with cortical slow oscillation up-states, but not out-of-phase-induced spindles, improve consolidation of hippocampus-dependent memory during sleep. Whereas optogenetically stimulated spindles were as efficient as spontaneous spindles in nesting hippocampal ripples within their excitable troughs, stimulation in-phase with the slow oscillation up-state increased spindle co-occurrence and frontal spindle-ripple co-occurrence, eventually resulting in increased triple coupling of slow oscillation-spindle-ripple events. In-phase optogenetic suppression of thalamic spindles impaired hippocampus-dependent memory. Our results suggest a causal role for thalamic sleep spindles in hippocampus-dependent memory consolidation, conveyed through triple coupling of slow oscillations, spindles, and ripples. Latchoumane et al. demonstrate a causal role of sleep spindles in memory formation. They show that optogenetic induction of thalamic spindles, when phase-locked to the slow oscillation up-state, enhances the triple coupling of slow oscillations-spindles-ripples together with hippocampus-dependent memory consolidation.
AB - While the interaction of the cardinal rhythms of non-rapid-eye-movement (NREM) sleep—the thalamo-cortical spindles, hippocampal ripples, and the cortical slow oscillations—is thought to be critical for memory consolidation during sleep, the role spindles play in this interaction is elusive. Combining optogenetics with a closed-loop stimulation approach in mice, we show here that only thalamic spindles induced in-phase with cortical slow oscillation up-states, but not out-of-phase-induced spindles, improve consolidation of hippocampus-dependent memory during sleep. Whereas optogenetically stimulated spindles were as efficient as spontaneous spindles in nesting hippocampal ripples within their excitable troughs, stimulation in-phase with the slow oscillation up-state increased spindle co-occurrence and frontal spindle-ripple co-occurrence, eventually resulting in increased triple coupling of slow oscillation-spindle-ripple events. In-phase optogenetic suppression of thalamic spindles impaired hippocampus-dependent memory. Our results suggest a causal role for thalamic sleep spindles in hippocampus-dependent memory consolidation, conveyed through triple coupling of slow oscillations, spindles, and ripples. Latchoumane et al. demonstrate a causal role of sleep spindles in memory formation. They show that optogenetic induction of thalamic spindles, when phase-locked to the slow oscillation up-state, enhances the triple coupling of slow oscillations-spindles-ripples together with hippocampus-dependent memory consolidation.
UR - http://www.scopus.com/inward/record.url?scp=85021793353&partnerID=8YFLogxK
U2 - 10.1016/j.neuron.2017.06.025
DO - 10.1016/j.neuron.2017.06.025
M3 - Journal articles
C2 - 28689981
AN - SCOPUS:85021793353
SN - 0896-6273
VL - 95
SP - 424-435.e6
JO - Neuron
JF - Neuron
IS - 2
ER -