TY - JOUR
T1 - Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall
AU - Dickey, Charles W.
AU - Verzhbinsky, Ilya A.
AU - Jiang, Xi
AU - Rosen, Burke Q.
AU - Kajfez, Sophie
AU - Stedelin, Brittany
AU - Shih, Jerry J.
AU - Ben-Haim, Sharona
AU - Raslan, Ahmed M.
AU - Eskandar, Emad N.
AU - Gonzalez-Martinez, Jorge
AU - Cash, Sydney S.
AU - Halgren, Eric
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank Adam Niese, Christine Smith, Christopher Gonzalez, Daniel Cleary, Eran Mukamel, Erik Kaestner, Jacob Garrett, Maxim Baz-henov, Terrence Sejnowski, and Zarek Siegel for their support. This work was supported by the National Institute of Mental Health (1RF1MH117155-01 and T32 MH020002) and the Office of Naval Research Multidisciplinary University Research Initiative (N00014-16-1-2829). Portions of this article were developed from the original doctoral dissertation by C.W.D.
Publisher Copyright:
Copyright © 2022 the Author(s).
PY - 2022/7/12
Y1 - 2022/7/12
N2 - 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 ∼70-ms-duration, 90-Hz ripples often couple (within ±500 ms), co-occur (≥ 25-ms 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 corippling. 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 coripples increase preceding successful delayed memory recall, when binding between the cue and response is essential. Ripples increase and phase-modulate unit firing, and coripples 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 (25 cm). Hippocampo-cortico-cortical coripples appear to possess the essential properties necessary to support binding by synchrony during memory retrieval and perhaps generally in cognition.
AB - 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 ∼70-ms-duration, 90-Hz ripples often couple (within ±500 ms), co-occur (≥ 25-ms 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 corippling. 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 coripples increase preceding successful delayed memory recall, when binding between the cue and response is essential. Ripples increase and phase-modulate unit firing, and coripples 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 (25 cm). Hippocampo-cortico-cortical coripples appear to possess the essential properties necessary to support binding by synchrony during memory retrieval and perhaps generally in cognition.
KW - cortex
KW - hippocampus
KW - non-rapid eye movement sleep
KW - ripples
KW - waking
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U2 - 10.1073/pnas.2107797119
DO - 10.1073/pnas.2107797119
M3 - Article
C2 - 35867767
AN - SCOPUS:85133878474
SN - 0027-8424
VL - 119
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 28
M1 - e2107797119
ER -