Functional microstates within human REM sleep: first evidence from fMRI of a thalamocortical network specific for phasic REM periods

Abstract

High thalamocortical neuronal activity characterizes both, wakefulness and rapid eye movement (REM) sleep, but apparently this network fulfills other roles than processing external information during REM sleep. To investigate thalamic and cortical reactivity during human REM sleep, we used functional magnetic resonance imaging with simultaneous polysomnographic recordings while applying acoustic stimulation. Our observations indicate two distinct functional substates within general REM sleep. Acoustic stimulation elicited a residual activation of the auditory cortex during tonic REM sleep background without rapid eye movements. By contrast, periods containing bursts of phasic activity such as rapid eye movements appear characterized by a lack of reactivity to sensory stimuli. We report a thalamocortical network including limbic and parahippocampal areas specifically active during phasic REM periods. Thus, REM sleep has to be subdivided into tonic REM sleep with residual alertness, and phasic REM sleep with the brain acting as a functionally isolated and closed intrinsic loop.

Human brain activity time-locked to rapid eye movements during REM sleep

“…In this line of thought, it is interesting to note that we found no signiWcant activation in the hippocampus, though both the amygdala and parahippocampal gyrus were activated. Although the reason for the inactivity of the hippocampus is not clear, this result is consistent with many recent PET (Maquet et al 1996;Braun et al 1998;Peigneux et al 2001) and fMRI (Wehrle et al 2007) studies. A second possibility is that these activations relate to the generation and maintenance of dream imagery.…”

“…A recent fMRI study also shows that a thalamocortical network including limbic and parahippocampal areas is speciWcally active during phasic REM periods (Wehrle et al 2007). Our present event-related fMRI study supports and extends this notion.…”

“…In addition, a recent fMRI study succeeded in separating two distinct functional sub-states (tonic and phasic periods) within REM sleep in humans (Wehrle et al 2007). Nevertheless, the lack of temporal resolution makes PET scans and non-event-related fMRI analysis unable to distinguish between tonic activations throughout REM sleep and phasic activations temporally related to REMs.…”

Cognitive and emotional processes during dreaming: A neuroimaging view

“…Yet, some recent fMRI studies suggest that rapid eye movements during REM sleep might be associated with increased fMRI activity in V1 (Miyauchi, Misaki, Kan, Fukunaga, & Koike, 2009). On the other hand, because several studies found that auditory stimuli may be processed to some extent during sleep (Atienza, Cantero, & Escera, 2001;Czisch et al, 2002;Perrin, Garcia-Larrea, Mauguiere, & Bastuji, 1999;Portas et al, 2000;Wehrle et al, 2007), we would predict that external auditory stimulation during sleep may effectively coordinate activation within primary and associative auditory cortices.…”

EEG-defined functional microstates as basic building blocks of mental processes

“…Several studies have shown that the temporal structure of the microstates changes as a function of the conscious/mental state of the subject, such as sleep (Wehrle et al, 2007), hypnosis (Katayama et al, 2007), centrally active medication , and mental disorders such as dementia (Strik et al, 1997), depression (Strik et al, 1995), and schizophrenia (Koenig et al, 1999;Strelets et al, 2003). In schizophrenia, a reduction in microstate duration and aberrant sequencing of the microstates has been described (Lehmann et al, 2005).…”