Slow EEG rhythms and inter-hemispheric synchronization across sleep and wakefulness in the human hippocampus

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Abstract

Converging data that attribute a central role to sleep in memory consolidation have increased the interest to understand the characteristics of the hippocampal sleep and their relations with the processing of new information. Neural synchronization between different brain regions is thought to be implicated in long-term memory consolidation by facilitating neural communication and by promoting neural plasticity. However, the majority of studies have focused their interest on intra-hippocampal, rhinal–hippocampal or cortico-hippocampal synchronization, while inter-hemispheric synchronization has been so far neglected.

To clarify the features of spontaneous human hippocampal activity and to investigate inter-hemispheric hippocampal synchronization across vigilance states, pre-sleep wakefulness and nighttime sleep were recorded from right and left homologous hippocampal loci using stereo-EEG techniques. Hence, quantitative and inter-hemispheric coherence analyses of hippocampal activity across sleep and waking states were carried out.

The results showed the presence of delta activity in human hippocampal spontaneous EEG also during wakefulness. The activity in the delta range exhibited a peculiar bimodal distribution, namely a low frequency non-oscillatory activity (up to 2 Hz) synchronized between hemispheres mainly during wake and REM sleep, and a faster oscillatory rhythm (2–4 Hz). The latter was less synchronized between the hippocampi and seemed reminiscent of animal RSA (rhythmic slow activity). Notably, the low-delta activity showed high inter-hemispheric hippocampal coherence during REM sleep and, to a lesser extent, during wakefulness, paralleled by a (unexpected) decrease of coherence during NREM sleep.

Therefore, low-delta hippocampal state-dependent synchronization starkly contrasts with neocortical behavior in the same frequency range. Further studies might shed light on the role of these low frequency rhythms in the encoding processes during wakefulness and in the consolidation processes during subsequent sleep.

Highlights

□ We found delta activity in the human hippocampus across all vigilance states. □ Two types of delta activity are originated in the hippocampus. □ Low delta is synchronous between the hippocampi during the activated states. □ High delta is weakly in phase between hemispheres. □ High delta is an oscillatory background rhythm while low delta is a transient rhythm.

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