Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: An intracranial electroencephalographic study

Abstract

Sleep is punctuated by transient elevations of vigilance level called arousals or awakenings depending on their durations. Understanding the dynamics of brain activity modifications during these transitional phases could help to better understand the changes in cognitive functions according to vigilance states. In this study, we investigated the activity of memory‐related areas (hippocampus and orbitofrontal cortex) during short (3 s to 2 min) arousing reactions detected from thalamic activity, using intracranial recordings in four drug‐resistant epilepsy patients. The average power of the signal between 0.5 and 128 Hz was compared across four time windows: 10 s of preceding sleep, the first part and the end of the arousal/awakening, and 10 s of wakefulness. We observed that (a) in most frequency bands, the spectral power during hippocampal arousal/awakenings is intermediate between wakefulness and sleep whereas frontal cortex shows an early increase in low and fast activities during non‐rapid‐eye‐movement (NREM) sleep arousals/awakenings; (b) this pattern depends on the preceding sleep stage with fewer modifications for REM than for non‐REM sleep arousal/awakenings, potentially reflecting the EEG similarities between REM sleep and wakefulness; (c) a greater activation at the arousing reaction onset in the prefrontal cortex predicts longer arousals/awakenings. Our findings suggest that hippocampus and prefrontal arousals/awakenings are progressive phenomena modulated by sleep stage, and, in the neocortex, by the intensity of the early activation. This pattern of activity could underlie the link between sleep stage, arousal/awakening duration and restoration of memory abilities including dream recall.

Spotlight on Sleep Stage Classification Based on EEG

“… 31 Beyond sleep onset, SEEG studies have shown that regional differences in EEG sleep/wake patterns persisted during whole-night sleep and were also observed during the sleep-to-wake transition. 32 , 33 In addition, specific sleep oscillation also exhibit regional specificities and disparities, as reported for NREM sleep spindles in the neocortex 34 , 35 and in the thalamus, 36 as well as for REM sleep sawtooth waves 37 and NREM sleep slow waves, 38 similarly to what was previously published in rodents. 39 Interestingly, local slow waves have also been detected in awake animals, leading to the concept of “local sleep”, 40 a mechanism hypothesized as causing attentional lapses in humans.…”

Tailoring Human Sleep: selective alteration through Brainstem Arousal Circuit Stimulation

“…When overt wakefulness occurred, the stimulation trial was terminated, while upon the observation of either stage shifts or Intra-Sleep Awakening Reactions (ISARs), the total duration of stimulation was limited to up to 3 minutes. These ISARs were defined as an abrupt, fast EEG frequency shift (including theta, alpha or frequency greater than 16 Hz with exclusion of spindles) following ten seconds of stable sleep, lasting more than ten seconds and followed by return to sleep 31,32 . Further details on assessment of sleep fragmentation in baseline recordings can be found in ‘Supplementary Materials’.…”

Relationship Between Epilepsy and Dreaming: Current Knowledge, Hypotheses, and Perspectives

“…Finally, our team (CRNL) and other colleagues have emphasized the role of awakenings in dream recall whose frequency/duration and efficiency (in terms of memory encoding) would depend on a specific activity notably in the default mode network during sleep and at awakening (Eichenlaub et al, 2014a,b;Vallat et al, 2017bVallat et al, , 2020Van Wyk et al, 2019). According to these works and to the "arousal-retrieval" model (Koulack and Goodenough, 1976), dream recall would require an awakening when the short-term memory of the dream experience is still "alive" and would depend on the brain's ability to return to a cognitive functioning closer to the waking state Ruby et al, 2021). This hypothesis which gives an important role to short-term memory in dream recall, is coherent with results showing that short-term memory [involving the prefrontal cortex, (Nee and Jonides, 2008)] is at least partially preserved in N2 and REM sleep, even if dlPFC possible deactivation during sleep may diminish its capacity and duration (Daltrozzo et al, 2012).…”