Abstract
Sleep oscillations in the neocortex and hippocampus are critical for the integration of new memories into stable generalized representations in neocortex. However, the role of the thalamus in this process is poorly understood. To determine the thalamic contribution to non-REM oscillations (sharp-wave ripples, SWRs; slow/delta; spindles), we recorded units and local field potentials (LFPs) simultaneously in the limbic thalamus, mPFC, and CA1 in rats. We report that the cycles of neocortical spindles provide a key temporal window that coordinates CA1 SWRs with sparse but consistent activation of thalamic units. Thalamic units were phase-locked to delta and spindles in mPFC, and fired at consistent lags with other thalamic units within spindles, while CA1 units that were active during spatial exploration were engaged in SWR-coupled spindles after behavior. The sparse thalamic firing could promote an incremental integration of recently acquired memory traces into neocortical schemas through the interleaved activation of thalamocortical cells.
Highlights
Two complementary learning systems acquire and process episodic memories in order to learn adaptive models of the world that generalize beyond specific experiences and continue to incorporate information through the lifetime of an animal[1–4]
We used tetrodes to record extracellularly from the midline thalamus, and from areas involved in recent (CA1) and remote memory recall[32,42]
local field potentials (LFPs) and 317 units were recorded from 7 rats; sessions from an additional animal in which no units were recorded were included for LFP analyses for a total of n = 8 rats (Figure 1a displays a subset of tetrode locations in brain sections from one rat; Supplementary Figure 1, parts 1 and 2, document the trajectories in the brain for the electrodes and sessions used for analyses)
Summary
Two complementary learning systems acquire and process episodic memories in order to learn adaptive models of the world that generalize beyond specific experiences and continue to incorporate information through the lifetime of an animal[1–4]. The hippocampus can form memory traces rapidly; over time, interactions between the hippocampus and neocortex are thought to extract statistical regularities from the organism’s experiences during wakefulness, and update neocortical models or schemas to increase their adaptive value[5,6]. During non-REM sleep, the interactions between the hippocampal and neocortical cell ensembles that underlie these processes are reflected in nested oscillations in the local field potentials (LFPs). Some cells are preferentially active at the start or at the end of upstates[7,8], and in the hippocampal CA1 region, sharpwave ripple oscillations (SWRs, 100–275 Hz) occur primarily during up-states[9]. The role of spindles in gating and coordinating multi-region communication remains to be explored at the cellular and systems level
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