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Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall

By Charles W Dickey, Ilya A Verzhbinsky, Xi Jiang, Burke Q Rosen, Sophie Kajfez, Brittany Stedelin, Jerry J Shih, Sharona Ben-Haim, Ahmed M Raslan, Emad N Eskandar, Jorge Gonzalez-Martinez, Sydney S Cash, Eric Halgren

Posted 24 Feb 2021
bioRxiv DOI: 10.1101/2021.02.23.432582

Declarative memory encoding, consolidation, and retrieval require the integration of elements encoded in widespread cortical locations. The mechanism whereby such 'binding' of different components of mental events into unified representations occurs is unknown. The 'binding-by-synchrony' theory proposes that distributed encoding areas are bound by synchronous oscillations enabling enhanced communication. However, evidence for such oscillations is sparse. Brief high-frequency oscillations ('ripples') occur in the hippocampus and cortex, and help organize memory recall and consolidation. Here, using intracranial recordings in humans, we report that these ~70ms duration 80Hz ripples often couple ({+/-}500ms), co-occur ([≥]25ms overlap), and crucially, phase-lock (have consistent phase-lags) between widely distributed focal cortical locations during both sleep and waking, even between hemispheres. Cortical ripple co-occurrence is facilitated through activation across multiple sites, and phase-locking increases with more cortical sites co-rippling. Ripples in all cortical areas co-occur with hippocampal ripples but do not phase-lock with them, further suggesting that cortico-cortical synchrony is mediated by cortico-cortical connections. Ripple phase-lags vary across sleep nights, consistent with participation in different networks. During waking, we show that hippocampo-cortical and cortico-cortical co-ripples increase preceding successful delayed memory recall, when binding between the cue and response is essential. Ripples increase and phase-modulate unit-firing, and co-ripples increase high-frequency correlations between areas, suggesting synchronized unit-spiking facilitating information exchange. Co-occurrence, phase-synchrony, and high-frequency correlation are maintained with little decrement over very long distances (25cm). Hippocampo-cortico-cortical co-ripples appear to possess the essential properties necessary to support binding-by-synchrony during memory retrieval, and perhaps generally.

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