Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents

Seibt, Julie; Richard, Clément J.; Sigl‐Glöckner, Johanna; Takahashi, Naoya; Kaplan, D.; Doron, Guy; Limoges, Denis de; Bocklisch, Christina; Larkum, Matthew E.

doi:10.1038/s41467-017-00735-w

Cited by 127 publications

(151 citation statements)

References 44 publications

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“…In humans, NC-SS (Hagler et al, 2018), and especially NC-SS/US increase firing (Csercsa et al, 2010;Mak-McCully et al, 2017;Gonzalez et al, 2018). In rodents, NC-SS (Seibt et al, 2017), and especially NC-SS/US (Niethard et al, 2018), are associated with strong Ca 2+ influx in NC pyramidal cell apical dendrites, and increased plasticity (Steriade and Timofeev, 2003). Behavioral consolidation in rodents depends on NC-SS/US coupling with HC-SWR (Maingret et al, 2016;Latchoumane et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Posterior hippocampal spindle-ripples co-occur with neocortical theta-bursts and down-upstates, and phase-lock with parietal spindles during NREM sleep in humans

Jiang

González-Martínez

Halgren

2019

Preprint

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Human anterior and posterior hippocampus (aHC, pHC) differ in connectivity and behavioral correlates. Here we report physiological differences. During NREM sleep, the human hippocampus generates sharpwave-ripples (SWR) similar to those which in rodents mark memory replay. We show that while pHC generates SWR, it also generates about as many spindle-ripples (SSR: ripples phase-locked to local spindles). In contrast, SSR are rare in aHC. Like SWR, SSR often co-occur with neocortical theta bursts (TB), downstates (DS), spindles (SS) and upstates (US), which coordinate cortico-hippocampal interactions and facilitate consolidation in rodents. SWR co-occur with these waves in widespread cortical areas, especially fronto-central. These waves typically occur in the sequence TB-DS-SS-US, with SWR usually occurring prior to SS-US. In contrast, SSR occur ~350 ms later, with a strong preference for cooccurrence with posterior-parietal SS. pHC-SS were strongly phase-locked with parietal-SS, and pHC-SSR were phase-coupled with pHC-SS and parietal-SS. Human SWR (and associated replay events, if any) are separated by ~5 s on average, whereas ripples on successive SSR peaks are separated by only ~80 ms. These distinctive physiological properties of pHC-SSR enable an alternative mechanism for hippocampal engagement with neocortex. Significance StatementRodent hippocampal neurons replay waking events during sharpwave-ripples in NREM sleep, facilitating memory transfer to a permanent cortical store. We show that human anterior hippocampus also produces sharpwave-ripples, but spindle-ripples predominate in posterior. Whereas sharpwave-ripples typically occur as cortex emerges from inactivity, spindle-ripples typically occur at peak cortical activity. Furthermore, posterior hippocampal spindle-ripples are tightly coupled to posterior parietal locations activated by conscious recollection. Finally, multiple spindle-ripples can recur within a second, whereas sharpwave-ripples are separated by about 5s. The human posterior hippocampus is considered homologous to rodent dorsal hippocampus, which is thought to be specialized for consolidation of specific memory details. We speculate that these distinct physiological characteristics of posterior hippocampal spindleripples may support a related function in humans.

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Section: Discussionmentioning

confidence: 99%

Posterior hippocampal spindle-ripples co-occur with neocortical theta-bursts and down-upstates, and phase-lock with parietal spindles during NREM sleep in humans

Jiang

González-Martínez

Halgren

2019

Preprint

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“…While the link between each of these sleep signatures and effective consolidation has been established across species [20,21,26,[30][31][32][33], less is known about their dynamic interactions underlying the purported information transfer from hippocampus to neocortex [5]. In particular, it has been argued that sleep spindles might be pivotal for facilitating hippocampal-neocortical interactions, opening fine-tuned windows of opportunity for cross-regional synchronisation and plasticity [10,11,22,[34][35][36]. In other words, spindles might serve as the mechanistic vehicle to synchronise the hippocampus with neocortical target sites at the time of hippocampal memory reactivation, i.e., around SW-Rs.…”

Section: Discussionmentioning

confidence: 99%

“…Triggered by SOs, the thalamus generates sleep spindles, i.e., transient (0.5-2 s) oscillatory activity between [12][13][14][15][16] Hz, via thalamo-cortical loops [8]. Nested in SO up-states, spindles gate Ca 2+ influx into dendrites and promote synaptic plasticity [9][10][11]. Importantly, spindles have also been shown to group hippocampal sharp-wave ripples (SW-Rs) [12][13][14].…”

Section: Introductionmentioning

confidence: 99%

Sleep spindles mediate hippocampal-neocortical coupling during sharp-wave ripples

Ngo

Fell

Staresina

2019

Preprint

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Sleep is pivotal for the consolidation of memories [1]. According to two-stage accounts, experiences are temporarily stored in the hippocampus and gradually translocated to neocortical sites during nonrapid-eye-movement (NREM) sleep [2,3]. Mechanistically, information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. In particular, spindles may open precisely-timed communication channels, across which reactivation patterns may travel between the hippocampus and cortical target sites when ripples occur. To test this hypothesis, we first derived time-frequency representations (TFRs) in hippocampus (HIPP) and at scalp electrode Cz (neocortex, NC) time-locked to individual hippocampal ripple events. Compared to matched ripplefree intervals, results revealed a concurrent increase in spindle power both in HIPP and NC. As revealed by coherence analysis, hippocampal-neocortical coupling was indeed enhanced in the spindle band around ripples. Finally, we examined the directionality of spindle coupling and observed a strong driving effect from NC to HIPP. Specifically, ~250 ms prior to the HIPP ripple, NC spindles emerge and entrain HIPP spindles. Both regions then remain synchronised until ~500 ms after the ripple.Consistent with recent rodent work, these findings suggest that active consolidation is initiated by neocortex and draws on neocortical-hippocampal-neocortical reactivation loops [4], with a role of sleep spindles in mediating this process.

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“…NC-SS tend to occur on the US, with elevated NC-SS density being recently shown to correlate with targeted memory reactivation in humans (Cairney et al, 2018). There is also a phasic additional increase in firing at SS peaks (Gonzalez et al, 2018), which together with a strong apical dendritic Ca +2 influx (Seibt et al, 2017;Niethard et al, 2018) would create the conditions for Spike Timing Dependent Plasticity (Froemke and Dan, 2002). Thus, if, as in rodents, human HC-SWR index the replay by HC pyramidal cells of firing sequences from the preceding waking, then our results imply that the information encoded in these firing patterns arrives in an NC prepared to construct firing patterns and consolidate the consequent networks by virtue of the coincident NC-SS and NC-US.…”

Section: Temporal Organization Of Hc-swr Interactions With Nc-gementioning

confidence: 99%

Coordination of human hippocampal sharpwave-ripples during NREM sleep with cortical theta bursts, spindles, downstates and upstates

Jiang

González-Martínez

Halgren

2019

Preprint

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In rodents, waking firing patterns replay in NREM sleep during hippocampal sharpwave-ripples (HC-SWR), correlated with neocortical graphoelements (NC-GE). NC-GE include theta-bursts, spindles, downstates and upstates. In humans, consolidation during sleep is correlated with scalprecorded spindles and down-upstates, but HC-SWR cannot be recorded non-invasively. Here we show in humans of both sexes that HC-SWR are highly correlated with NC-GE during NREM, with significantly more related HC-SWR/NC-GE for downstates or upstates than theta-bursts or spindles, in N2 than N3, in posterior than anterior HC, in frontal than occipital cortex, and ipsilaterally than contralaterally. The preferences interacted, e.g. frontal spindles co-occurred frequently with posterior HC-SWR in N2. These preferred GE, stages and locations for HC-SWR/NC-GE interactions may index selective consolidation activity, although that was not tested in this study. SWR recorded in different HC regions seldom co-occurred, and were related to GE in different cortical areas, showing that HC-NC interact in multiple transient, widespread but discrete, networks. NC-GE tend to occur with consistent temporal relationships to HC-SWR, and to each other. Cortical theta-bursts usually precede HC-SWR, where they may help define cortical input triggering HC-SWR firing. HC-SWR often follow cortical downstate onsets, surrounded by locally-decreased broadband power, suggesting a mechanism synchronizing cortical, thalamic and hippocampal activities. Widespread cortical upstates and spindles follow HC-SWR, consistent with the hypothesized contribution by hippocampal firing during HC-SWR to cortical firing-patterns during upstates and spindles. Overall, our results describe how hippocampal and cortical oscillations are coordinated in humans during events that are critical for memory consolidation in rodents. Significance Statement:Hippocampal sharpwave-ripples, essential for memory consolidation, mark when hippocampal neurons replay waking firing patterns. In rodents, cortical sleep waves coordinate the transfer of temporary hippocampal to permanent cortical memories, but their relationship with human HC-SWR remains unclear. We show that human hippocampal sharpwave-ripples co-occur with all varieties of cortical sleep waves, in all cortical regions, and in all stages of Non-REM sleep but with overall preferences for each of these. We found that sharpwave-ripples in different parts of the hippocampus usually occurred independently of each other, and preferentially interacted with different cortical areas. We found that sharpwave-ripples typically occur after certain types of cortical waves, and before others, suggesting how the cortico-hippocampo-cortical interaction may be organized in time and space.

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Cortical dendritic activity correlates with spindle-rich oscillations during sleep in rodents

Cited by 127 publications

References 44 publications

Posterior hippocampal spindle-ripples co-occur with neocortical theta-bursts and down-upstates, and phase-lock with parietal spindles during NREM sleep in humans

Posterior hippocampal spindle-ripples co-occur with neocortical theta-bursts and down-upstates, and phase-lock with parietal spindles during NREM sleep in humans

Sleep spindles mediate hippocampal-neocortical coupling during sharp-wave ripples

Coordination of human hippocampal sharpwave-ripples during NREM sleep with cortical theta bursts, spindles, downstates and upstates

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