Phase-based coordination of hippocampal and neocortical oscillations during human sleep

Cox, Roy; Rüber, Theodor; Staresina, Bernhard P.; Fell, Juergen

doi:10.1101/745745

Cited by 1 publication

(2 citation statements)

References 85 publications

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“…1CD). These findings extend observations of spindle synchrony between HPC and NC (14,16,29), or within NC (30), involving AMY in a widespread network of spindle-related coordination. Moreover, we observed several instances in which ripples were associated with locally enhanced spindle activity in both AMY and HPC.…”

Section: Discussionsupporting

confidence: 88%

“…For all contact pairs, the more posterior contact was considered the active electrode, and the more anterior one the reference. Distance between HPC and AMY channel pairs was 31.5 ± 3.7 mm (range: [27][28][29][30][31][32][33][34][35][36]. Additional non-invasive signals were recorded from the scalp (Cz, C3, C4, Oz, A1, A2), the outer canthi of the eyes for electrooculography (EOG), and chin for electromyography (EMG).…”

Section: Data Acquisitionmentioning

confidence: 99%

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Sharp wave-ripples in human amygdala and their coordination with hippocampus during NREM sleep

Cox

Rüber

Staresina

et al. 2020

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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 intracranial recordings in four pre-surgical epilepsy patients, we discovered ripples within human amygdala during non-rapid eye movement sleep. Like hippocampal ripples, amygdala ripples are strongly associated with sharp waves, are linked to sleep spindles, and tend to co-occur with their hippocampal counterparts. Moreover, sharp waves and ripples are temporally linked across the two 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 sleep-dependent consolidation and regulation of emotional experiences.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 (2-5). 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). In contrast, while human neuroimaging studies indicate enhanced AMY-HPC communication during emotional memory retrieval after sleep compared to wake (7), direct evidence for AMY-HPC communication during human sleep is surprisingly absent.Ripples, ~80 Hz oscillations found in human HPC (8) and various neocortical (NC) areas (9-13), are of potential interest for such AMY-HPC interactions. Sharp wave-ripple complexes in HPC (SPW-ripples; ripples superimposed on ~3 Hz sharp waves), mediate widespread communication between . In animals, neuronal replay preferentially occurs during SPW-ripples (17), and suppressing SPW-ripples impairs memory consolidation (18). Importantly, the aforementioned AMY-HPC replay underlying emotional memory consolidation similarly coincides with HPC SPW-ripples (6), pointing to a key role for ripples in the AMY-HPC dialog. Of note, 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.Beside their close association with SPWs, HPC ripples are nested within HPC and NC ~13 Hz sleep spindles and ~1 Hz slow oscillations (SOs) (8, 21), enhancing HPC-NC information exchange and consolidation (16,22,23). Whether these additional oscillatory rhythms have a role to play in AMY-HPC communication, either on their own or in conjunction with ripples, also remains unexplored. Here. we report the existence of SPW-ripples in human AMY, and bidirectional AMY-HPC ripple, SPW, and spindle interactions during NREM sleep, offering a potential physiological basis for various...

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Section: Discussionsupporting

confidence: 88%