Human amygdala activation during rapid eye movements of rapid eye movement sleep: an intracranial study

Abstract

The amygdaloid complex plays a crucial role in processing emotional signals and in the formation of emotional memories. Neuroimaging studies have shown human amygdala activation during rapid eye movement sleep (REM). Stereotactically implanted electrodes for presurgical evaluation in epileptic patients provide a unique opportunity to directly record amygdala activity. The present study analysed amygdala activity associated with REM sleep eye movements on the millisecond scale. We propose that phasic activation associated with rapid eye movements may provide the amygdala with endogenous excitation during REM sleep. Standard polysomnography and stereo-electroencephalograph (SEEG) were recorded simultaneously during spontaneous sleep in the left amygdala of four patients. Time-frequency analysis and absolute power of gamma activity were obtained for 250 ms time windows preceding and following eye movement onset in REM sleep, and in spontaneous waking eye movements in the dark. Absolute power of the 44-48 Hz band increased significantly during the 250 ms time window after REM sleep rapid eye movements onset, but not during waking eye movements. Transient activation of the amygdala provides physiological support for the proposed participation of the amygdala in emotional expression, in the emotional content of dreams and for the reactivation and consolidation of emotional memories during REM sleep, as well as for next-day emotional regulation, and its possible role in the bidirectional interaction between REM sleep and such sleep disorders as nightmares, anxiety and post-traumatic sleep disorder. These results provide unique, direct evidence of increased activation of the human amygdala time-locked to REM sleep rapid eye movements.

Mild Traumatic Brain Injury Chronically Impairs Sleep- and Wake-Dependent Emotional Processing

“…67 Recent evidence suggests activation of the amygdala occurs predominantly after REM bursts during REM sleep. 68 Thus, a reduction in REM should limit amygdala activation, reducing the sleep-dependent "boost" for emotional stimuli.…”

Smiling asleep: A study of happy emotional expressions during adult sleep

“…The measure started 5 s before the event, as this is a common time window for a baseline analysis of heart rate changes before and after motor events such as periodic leg movements (Pennestri et al, 2013). Because rapid eye movements (REMs) in REM sleep are temporally locked with the activity in the amygdala (Andrillon, Nir, Cirelli, Tononi, & Fried, 2015;Calvo & Fernández-Guardiola, 1984;Corsi-Cabrera et al, 2016;Miyauchi, Misaki, Kan, Fukunaga, & Koike, 2009), we measured how frequently REMs exactly overlapped the zygomatic muscle activity in REM sleep. Eventually, we looked for behaviours associated with smiles and laughs to find scenic behaviours directly indicative of pleasant or unpleasant mental scenarios.…”

“…In addition, half of the smiles and laughs were temporally synchronized with REMs in REM sleep. Because REMs are associated with activation of the amygdala (the brain structure activated during awake emotions) in normal REM sleep (Andrillon et al, 2015;Calvo & Fernández-Guardiola, 1984;Corsi-Cabrera et al, 2016;Miyauchi et al, 2009), one may infer that many happy emotional expressions are associated with amygdala activation. Happy expressions were not associated with increased heart rate variability during sleep, as is sometimes observed when smiling while awake (Ekman et al, 1983).…”

The ‘affect tagging and consolidation’ (ATaC) model of depression vulnerability

“…Amygdala activations time-locked to REM sleep REMs have also been detected using stereoelectroencephalograph (SEEG; Corsi-Cabrera et al, 2016) and single-neuron recording (Andrillon, Nir, Cirelli, Tononi, & Fried, 2015) methods. These findings suggest that REM sleep density may be a surrogate marker of limbic neural activity during REM sleep, and might be associated with emotional memory processing.…”