Abstract
Cooperative interactions between the amygdala and hippocampus are widely regarded as critical for overnight emotional processing of waking experiences, but direct support from the human brain for such a dialog is absent. Using overnight intracranial recordings in 4 presurgical epilepsy patients (3 female), we discovered ripples within human amygdala during nonrapid eye movement (NREM) sleep, a brain state known to contribute to affective processing. Like hippocampal ripples, amygdala ripples are associated with sharp waves, linked to sleep spindles, and tend to co-occur with their hippocampal counterparts. Moreover, sharp waves and ripples are temporally linked across the 2 brain structures, with amygdala ripples occurring during hippocampal sharp waves and vice versa. Combined with further evidence of interregional sharp-wave and spindle synchronization, these findings offer a potential physiological substrate for the NREM-sleep-dependent consolidation and regulation of emotional experiences.
Highlights
Human sleep plays a pivotal role in emotional processing 1, including the consolidation of emotional memory traces, modulation of emotional reactivity, and regulation of general emotional well-being [2,3,4,5]
We analyzed invasive electroencephalography (EEG) during non-rapid eye movement (NREM) sleep from four patients (p1-p4) suffering from intractable epilepsy implanted with multi-contact depth electrodes
While ample behavioral evidence has established a critical role for sleep in emotional processing 1, it has remained unclear how these processes are implemented neurophysiologically
Summary
Human sleep plays a pivotal role in emotional processing 1, including the consolidation of emotional memory traces, modulation of emotional reactivity, and regulation of general emotional well-being [2,3,4,5]. Such sleep-dependent emotional processing is generally assumed to rely on coordinated activity between the amygdala (AMY) and hippocampus (HPC), as supported by joint AMY-HPC replay of threat-related spiking sequences during animal non-rapid eye movement (NREM) sleep 6. The aforementioned AMY-HPC replay underlying emotional memory consolidation coincides with HPC SPW-ripples 6, pointing to a key role for ripples in the AMY-HPC dialog. Ripple-like activity has been described in animal AMY 19,20, raising the possibility of coordinated ripples between these brain structures, but, importantly, ripples have never been described in human AMY
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