Large-Scale Microelectrode Recordings of High-Frequency Gamma Oscillations in Human Cortex during Sleep

Quyen, Michel Le Van; Staba, Richard J.; Bragin, Anatol; Dickson, Clayton T.; Valderrama, Mario; Fried, Itzhak; Engel, Jerome

doi:10.1523/jneurosci.5049-09.2010

Cited by 172 publications

(163 citation statements)

References 69 publications

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“…Although there is more δ-band power during SWS than wake (by definition), power in δ frequencies is present during wakefulness. Moreover, as has been previously reported, γ oscillations are present during wake and SWS (25).…”

Section: Significancesupporting

confidence: 82%

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Mitra

Snyder

Hacker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

110

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Declarative memory consolidation is hypothesized to require a twostage, reciprocal cortical-hippocampal dialogue. According to this model, higher frequency signals convey information from the cortex to hippocampus during wakefulness, but in the reverse direction during slow-wave sleep (SWS). Conversely, lower-frequency activity propagates from the information "receiver" to the "sender" to coordinate the timing of information transfer. Reversal of sender/ receiver roles across wake and SWS implies that higher-and lower-frequency signaling should reverse direction between the cortex and hippocampus. However, direct evidence of such a reversal has been lacking in humans. Here, we use human resting-state fMRI and electrocorticography to demonstrate that δ-band activity and infraslow activity propagate in opposite directions between the hippocampus and cerebral cortex. Moreover, both δ activity and infraslow activity reverse propagation directions between the hippocampus and cerebral cortex across wake and SWS. These findings provide direct evidence for state-dependent reversals in human cortical-hippocampal communication.D eclarative memories are initially hippocampus-dependent and gradually become hippocampus-independent over time, that is, consolidated (1, 2). It is theorized that a two-stage reciprocal dialogue between the hippocampus and the cerebral cortex underlies memory consolidation (3-5). According to this model, active behavior generates experiential codes in the cortex that are transmitted to the hippocampus, which houses a labile information store. Later, during slow-wave sleep (SWS), recently acquired hippocampal information is reactivated and transmitted to the cerebral cortex, where it is integrated into a more permanent memory store (5, 6). Thus, the hippocampus and cerebral cortex are proposed to exchange roles in sending and receiving information across wake and SWS (5, 6). Importantly, this model does not imply that all signals travel from the "sender" to the "receiver." Instead, the theory proposes that high-frequency activity carries information from the sender to receiver, that is, from the cortex to hippocampus or the hippocampus to cortex, depending on the stage of memory consolidation (wake or SWS, respectively) (4). Conversely, low-frequency activity propagates from the receiver back to the sender to coordinate the transfer of high-frequency information through modulation of the sender's excitability (4, 7-9). Hence, the two-stage reciprocal dialogue model predicts that lower and higher frequency activity between the hippocampus and cortex should propagate in opposite directions across wake and SWS, as illustrated in the schematic in Fig. 1. However, such reversal has not been directly observed in humans.We have recently analyzed temporal lags (delays) in neural signals to study the net propagation of spontaneous activity. In particular, we investigated resting-state fMRI (rs-fMRI) blood oxygen level-dependent (BOLD) signals and demonstrated directed propagation of infraslow activity (<0.1...

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Section: Significancesupporting

confidence: 82%

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Mitra

Snyder

Hacker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

110

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“…They can be evoked by various stimuli, as HFOs emerging from the somatosensory areas overlying the cortical response of the somatosensory evoked potential (Hashimoto, 2000;Ozaki and Hashimoto, 2011) or HFOs recorded from the nonepileptic occipital cortex and driven by visual tasks . A high frequency (80-120 Hz) gamma oscillation partially overlapping the frequency band of the continuous HFA has been previously reported in patients studied with large-scale microelectrode recordings in all investigated cortical areas during slow-wave sleep, in the form of short bursts, and speculated to briefly restore "microwake" activity important for memory traces consolidation (Le Van Quyen et al, 2010).…”

Section: Discussionmentioning

confidence: 86%

Continuous High Frequency Activity: A peculiar SEEG pattern related to specific brain regions

Melani

Zelmann

Mari

et al. 2013

Clinical Neurophysiology

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Objective-While visually marking the high frequency oscillations in the stereo-EEG of epileptic patients, we observed a continuous/semicontinuous activity in the ripple band (80-250 Hz), which we defined continuous High Frequency Activity (HFA). We aim to analyze in all brain regions the occurrence and significance of this particular pattern.Methods-Twenty patients implanted in mesial temporal and neocortical areas were studied. One minute of slow-wave sleep was reviewed. The background was classified as continuous/ semicontinuous, irregular, or sporadic based on the duration of the fast oscillations. Each channel was classified as inside/outside the seizure onset zone (SOZ) or a lesion.Results-The continuous/semicontinuous HFA occurred in 54 of the 790 channels analyzed, with a clearly higher prevalence in hippocampus and occipital lobe. No correlation was found with the SOZ or lesions. In the occipital lobe the continuous/semicontinuous HFA was present independently of whether eyes were open or closed. Conclusions-We describe what appears to be a new physiological High Frequency Activity, independent of epileptogenicity, present almost exclusively in the hippocampus and occipital cortex but independent of the alpha rhythm.Significance-The continuous HFA may be an intrinsic characteristic of specific brain regions, reflecting a particular type of physiological neuronal activity.

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“…It has been shown that coherent γ-oscillations are present during REM in magnetoencephalography (MEG) recordings (10). Evidence from extracranial EEG and iEEG recordings in epileptics shows that the synchrony of macroscopic γ is lower in SWS and REM relative to the awake state (27) and that γ-presence shows a phasic expression during SWS (11,28).…”

Section: Discussionmentioning

confidence: 99%

“…10). A recent study using microwires and intracranial electroencephalography (iEEG) recordings in the neocortex of epileptics has verified the strong presence of γ-oscillations during slow-wave sleep (SWS) (11). That study also showed a marked increase of spiking during γ, a suggestive indicator of association with cortical UP states.…”

mentioning

confidence: 89%

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

Quyen

Muller

Teleńczuk

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Beta (β)-and gamma (γ)-oscillations are present in different cortical areas and are thought to be inhibition-driven, but it is not known if these properties also apply to γ-oscillations in humans. Here, we analyze such oscillations in high-density microelectrode array recordings in human and monkey during the wake-sleep cycle. In these recordings, units were classified as excitatory and inhibitory cells. We find that γ-oscillations in human and β-oscillations in monkey are characterized by a strong implication of inhibitory neurons, both in terms of their firing rate and their phasic firing with the oscillation cycle. The β-and γ-waves systematically propagate across the array, with similar velocities, during both wake and sleep. However, only in slow-wave sleep (SWS) β-and γ-oscillations are associated with highly coherent and functional interactions across several millimeters of the neocortex. This interaction is specifically pronounced between inhibitory cells. These results suggest that inhibitory cells are dominantly involved in the genesis of β-and γ-oscillations, as well as in the organization of their large-scale coherence in the awake and sleeping brain. The highest oscillation coherence found during SWS suggests that fast oscillations implement a highly coherent reactivation of wake patterns that may support memory consolidation during SWS.excitation | inhibition | state-dependent firing | wave propagation | synchrony N eocortical beta (β)-and gamma (γ)-oscillations have been largely studied in the context of action/cognition during wakefulness (1-3). Although numerous studies have focused intensely on the information-processing role of β and γ during wakefulness, these rhythms do also occur during deep anesthesia and natural sleep (4-6). Additionally, although very-high-frequency allocortical oscillations (e.g., ripples at 80-200 Hz and fast ripples at 200-500 Hz in rodent/human hippocampus) have been thoroughly implicated in sleep-dependent memory consolidation (ref. 7 and reviewed in refs. 8 and 9), the occurrence and role of neocortical β-and γ-oscillations during sleep remain largely unexplored and related studies have been limited to macroscopic (whole-brain) scales (e.g., ref. 10). A recent study using microwires and intracranial electroencephalography (iEEG) recordings in the neocortex of epileptics has verified the strong presence of γ-oscillations during slow-wave sleep (SWS) (11). That study also showed a marked increase of spiking during γ, a suggestive indicator of association with cortical UP states. Here, we evaluate the presence of neocortical β-and γ-oscillations during the wake-sleep cycle at the level of local circuitry using dense 2D multielectrode recordings with identified excitatory and inhibitory cells (12, 13).Experimental and theoretical studies suggest that thalamocortical oscillations (including β and γ) are generated through a combination of intrinsic mechanisms involving the interplay between different ionic currents and extrinsic interaction of inhibitory and excitatory c...

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Large-Scale Microelectrode Recordings of High-Frequency Gamma Oscillations in Human Cortex during Sleep

Cited by 172 publications

References 69 publications

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Continuous High Frequency Activity: A peculiar SEEG pattern related to specific brain regions

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

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