Thalamic Spindles Promote Memory Formation during Sleep through Triple Phase-Locking of Cortical, Thalamic, and Hippocampal Rhythms

Charles Francois V. Latchoumane, Hong Viet V. Ngo, Jan Born*, Hee Sup Shin

*Corresponding author for this work
151 Citations (Scopus)

Abstract

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.

Original languageEnglish
JournalNeuron
Volume95
Issue number2
Pages (from-to)424-435.e6
ISSN0896-6273
DOIs
Publication statusPublished - 19.07.2017

Research Areas and Centers

  • Academic Focus: Center for Brain, Behavior and Metabolism (CBBM)

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