Abstract
During sleep, new memories undergo a gradual transfer from hippocampal (HPC) to neocortical (NC) sites. Precisely timed neural oscillations are thought to mediate this sleep-dependent memory consolidation, but exactly how sleep oscillations instantiate the HPC-NC dialog remains elusive. Employing overnight invasive electroencephalography in ten neurosurgical patients, we identified three broad classes of phase-based communication between HPC and lateral temporal NC. First, we observed interregional phase synchrony for non-rapid eye movement (NREM) spindles, and N2 and rapid eye movement (REM) theta activity. Second, we found asymmetrical N3 cross-frequency phase-amplitude coupling between HPC slow oscillations (SOs) and NC activity spanning the delta to high-gamma/ripple bands, but not in the opposite direction. Lastly, N2 theta and NREM spindle synchrony were themselves modulated by HPC SOs. These forms of interregional communication emphasize the role of HPC SOs in the HPC-NC dialog, and may offer a physiological basis for the sleep-dependent reorganization of mnemonic content.
Highlights
During sleep, new memories undergo a gradual transfer from hippocampal (HPC) to neocortical (NC) sites
(wPLI: a metric minimally sensitive to common neural sources69), we observed that raw weighted phase lag index (wPLI) showed a general decrease with frequency (Fig. 2a), with slower rhythms showing stronger synchrony than fast oscillations, as typically observed[70]
Assessing whether the phase of HPC rhythms coordinates faster activity in NC (“HPC-NC phase-amplitude coupling (PAC)”), we found that HPC slow oscillations (SOs) (0.5–1 Hz) robustly orchestrate the expression of faster activity in NC during N3 sleep (Fig. 3a)
Summary
New memories undergo a gradual transfer from hippocampal (HPC) to neocortical (NC) sites. Especially nonrapid eye movement (NREM) neocortical slow oscillations (SOs; 0.5–1.5 Hz), thalamocortical sleep spindles (12.5–16 Hz), and hippocampal ripples (60–100 Hz20–26; note that human ripples are substantially slower than ~150–250 Hz rodent ripples27,28), are widely held to mediate this HPC-NC memory transfer and consolidation process[29,30,31,32,33,34], given the presence of both SOs and spindles in HPC22,24,35–37. Various other spectral components exist in electrophysiological recordings of human sleep, with recent evidence suggesting potential roles for theta (4–8 Hz) in NREM38,39 and rapid eye movement (REM)[40,41] memory processing, complicating the question of which oscillatory rhythms instantiate the HPC-. Oscillatory phase (i.e., the relative position along the oscillatory cycle) has a critical influence on neuronal excitability and activity[42], thereby offering a precise temporal scaffold for orchestrating neural processing within and across brain structures[43,44]
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