Sharp Wave-Ripples in Human Amygdala and Their Coordination with Hippocampus during NREM Sleep

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 four pre-surgical epilepsy patients (three female), we discovered ripples within human amygdala during non-rapid 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 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 NREM-sleep-dependent consolidation and regulation of emotional experiences.

Slow oscillation‐spindle coupling is negatively associated with emotional memory formation following stress

“…Far less is known however about amygdala activity during SWS in humans. Recent research has shown that sharp-wave ripples occur in the human amygdala during SWS, and these are temporally linked with both ripples in the hippocampus and sleep spindles (though notably not slow oscillations) (Cox et al, 2020).…”

Slow oscillation-spindle coupling is negatively associated with emotional memory formation following stress

“…Far less is known however about amygdala activity during SWS in humans. Recent research has shown that sharp-wave ripples occur in the human amygdala during SWS, and these are temporally linked with both ripples in the hippocampus and sleep spindles (though notably not slow oscillations) (Cox et al , 2020). This provides a potential physiological basis for emotional memory consolidation during SWS, although an association with memory is yet to be reported.…”

“…A key distinction between neutral and emotional memory formation is the involvement of the amygdala (Payne & Kensinger, 2018). While theories of memory consolidation highlight dialogue between the hippocampus and neocortex during SWS as being involved in memory consolidation, interactions between the hippocampus and amygdala, and their relevance for behavior, is currently underexplored (though see Cox et al, 2020). Furthermore, many studies examining SWS in relation to memory focus exclusively on sleep stage correlations.…”

Long-Range GABAergic Projections of Cortical Origin in Brain Function

“…Notably, even the immobility-associated LRGN population in SO are heterogeneous, with some but not all cells showing activity that is phase-locked to sharp-wave ripples ( Katona et al, 2017 ; Francavilla et al, 2018 ). Interestingly, these HPC ripples are linked to memory consolidation in sleep ( Buzsaki, 2015 ; Oliva et al, 2020 ), potentially in coordination with cortical and subcortical regions ( Cox et al, 2020 ; Norimoto et al, 2020 ; Skelin et al, 2021 ). Thus, it is possible that HPC LRGNs may serve to synchronize activity in the HPC as well as in distributed brain regions in memory processing.…”