Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans

Abstract

How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.

Phase-based coordination of hippocampal and neocortical oscillations during human sleep

“…However, clear departures from this downward trend appeared for three main frequency bands. First, phase synchrony was enhanced in the spindle range (13.6-15.3 Hz) during N2 and especially N3 sleep, consistent with findings from other brain sites (36,39). Surprisingly, however, synchronization enhancements were also observed in the theta range (7.4-8.3 Hz) during N2 and REM, and in the beta range (28 Hz) during N3.…”

“…Sleep spindles are closely tied to memory and plasticity (17,18,64,65), and show widespread phase synchronization in neocortical networks (36). Here, we extend these observations of NREM spindle synchrony to include dynamics between HPC and lateral temporal cortex, similar to recent observations between HPC and prefrontal areas (39). Thus, the precise coordination of spindle activity across HPC and distributed neocortical areas may offer a potential mechanism to transiently reactivate distributed memory traces, and thereby contribute to NREM-dependent memory consolidation.…”

“…Other group-level effects of above-zero coupling were observed in the SO/delta range during REM (Puncorrected<0.05), and for N2 delta (Puncorrected<0.003). Interestingly, no SObased connectivity was seen during N2 or N3, suggesting that SO phase relations between HPC and NC are relatively variable (25,39).…”

“…First, consistent oscillatory phase locking between brain regions at the same frequency is thought to enable effective communication between the underlying neuronal groups (34). Phase synchrony during sleep has been reported between neocortical regions for various frequency bands (35), including the spindle (36,37) and gamma (38) ranges, and between HPC and prefrontal areas in the spindle range (39). Whether similar phenomena exist between human HPC and non-frontal NC areas, for which frequency bands, and in which sleep stages, has not been examined.…”

“…We hypothesized that these areas exhibit interregional phase coordination, which could manifest in any or all of the three aforementioned forms of coupling. Given both the theoretical importance of nested SO-spindle-ripple activity (52), and inconclusive evidence regarding the directionality of HPC-NC coupling (22,25,39,(53)(54)(55)(56)(57), we were particularly interested in whether HPC and NC SOs or spindles modulate faster activity at the other brain site, and if so, whether these effects are direction-dependent. Moreover, we considered a wide 0.5-200 Hz frequency range to allow potential identification of oscillatory communication lines outside the canonical SO-spindle-ripple framework.…”