Oscillating circuitries in the sleeping brain

Adamantidis, Antoine; Herrera, Carolina Gutierrez; Gent, Thomas C.

doi:10.1038/s41583-019-0223-4

Cited by 190 publications

(171 citation statements)

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“…The θ rhythm is primarily generated in the hippocampus (Adamantidis et al, 2019;Lubenov and Siapas, 2009) and is driven by GABAergic neurons in the medial septum firing at 4-8 Hz (Colgin, 2016). It is plausible that as EEG recovery continues following PGES, the emergence of θ waves may be an EEG indicator of continued post-ictal stupor and confusion.…”

Section: Increases In Sympathetic Tone and Decreases In Parasympathetmentioning

confidence: 99%

Post-ictal generalized EEG suppression and seizure-induced mortality are reduced by enhancing dorsal raphe serotonergic neurotransmission

Petrucci

Joyal

et al. 2020

Preprint

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AbstractSudden unexpected death in epilepsy (SUDEP) is the leading cause of death in patients with refractory epilepsy. A proposed risk marker for SUDEP is the duration of post-ictal generalized EEG suppression (PGES). The mechanisms underlying PGES are unknown. Serotonin (5-HT) has been implicated in SUDEP pathophysiology. Seizures suppress activity of 5-HT neurons in the dorsal raphe nucleus (DRN). We hypothesized that suppression of DRN 5-HT neuron activity contributes to PGES and increasing 5-HT neurotransmission or stimulating the DRN before a seizure would decrease PGES duration. Adult C57BL/6 and Pet1-Cre mice received EEG/EMG electrodes, a bipolar stimulating/recording electrode in the right basolateral amygdala, and either a microdialysis guide cannula or an injection of adeno-associated virus (AAV) allowing expression of channelrhodopsin2 plus an optic fiber into the DRN. Systemic application of the selective 5-HT reuptake inhibitor citalopram (20 mg/kg) decreased PGES duration from seizures induced during wake (n = 23) and NREM sleep (n = 13) whereas fluoxetine (20 mg/kg) pretreatment decreased PGES duration following seizures induced from wake (n = 11), but not NREM sleep (n = 9). Focal chemical (n = 6) or optogenetic (n = 8) stimulation of the DRN reduced PGES duration following kindled seizures and reduced morality following maximal electroshock seizures (n = 6) induced during wake. During PGES, animals exhibited immobility and suppression of EEG activity that was reduced by citalopram pretreatment. These results indicate that 5-HT and the DRN may regulate PGES and seizure-induced mortality.Highlights-PGES consistently follows seizures induced by amygdala stimulation in amygdala-kindled mice.-Seizure-induced dysregulation of 5-HT neurotransmission from the dorsal raphe nucleus may contribute to PGES.-Systemic administration of 5-HT enhancing drugs and stimulation of the DRN reduces PGES duration.-PGES is associated with post-ictal immobility in kindled mice that can be reduced by pretreatment with citalopram.-Recovery of EEG frequencies to baseline occurs in a stepwise manner with the lowest frequencies recovering first.

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Section: Increases In Sympathetic Tone and Decreases In Parasympathetmentioning

confidence: 99%

Post-ictal generalized EEG suppression and seizure-induced mortality are reduced by enhancing dorsal raphe serotonergic neurotransmission

Petrucci

Joyal

et al. 2020

Preprint

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“…States of vigilance in mammals are traditionally defined based on behavioural criteria and brain activity. [1][2][3] Sleep is typically defined as a state of relative immobility and reduced sensory responsiveness, while wakefulness is characterised by movement and active engagement with the environment. These characteristics of an awake state are thought to be essential for its main functions, including feeding, mating or defence against predation.…”

Section: Introductionmentioning

confidence: 99%

“…During wakefulness, cortical activity is characterised by fast, a low amplitude EEG dominated by activities in a theta-frequency range (6-9 Hz), whilst non-rapid eye movement (NREM) sleep is dominated by slow waves (typically 0.5-4 Hz), arising within thalamocortical networks. 1,10 The amplitude of slow-waves during NREM sleep is an established marker of the homeostatic sleep drive, which increases with prolonged wake and decreases with sleep. 11 By contrast, another state of sleeprapid eye-movement (REM) sleep -is typically characterised by lower amplitude, higher frequency, and theta-frequency oscillations, i.e.…”

Section: Introductionmentioning

confidence: 99%

“…similar to the waking state. 1 The sub-division of vigilance states into wake and sleep based on EEG and electromyography (EMG) signals and behaviour is relatively straightforward under physiological conditions, such as when the body temperature is normal (euthermic). 4 | P a g e However, significant deviation from normal body temperature may result in the occurrence of states that do not satisfy the criteria for wake and sleep established for euthermic conditions.…”

Section: Introductionmentioning

confidence: 99%

“…One of the most notable states is torpor, defined as a regulated and reversible state of metabolic suppression. 1,12,13 Torpor is used by many mammals as a strategy to conserve energy, particularly during periods of perceived or actual food shortage. 13…”

Section: Introductionmentioning

confidence: 99%

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The relationship between fasting-induced torpor, sleep and wakefulness in the laboratory mouse

Vyazovskiy

Peirson

Foster

et al. 2020

Preprint

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Torpor is a regulated reversible state of metabolic suppression used by many mammalian species to conserve energy. Although torpor has been studied extensively in terms of general physiology, metabolism and neuroendocrinology, the effects of hypometabolism and associated hypothermia on brain activity and states of vigilance have received little attention. Here we performed continuous monitoring of electroencephalogram (EEG), electromyogram (EMG) and peripheral body temperature in adult, male C57BL/6 mice over consecutive days of scheduled restricted feeding. All animals showed prominent bouts of hypothermia that became progressively deeper and longer as fasting progressed. EEG and EMG were markedly affected by hypothermia, although the typical electrophysiological signatures of NREM sleep, REM sleep and wakefulness allowed us to perform vigilance-state classification in all cases. Invariably, hypothermia bouts were initiated from a state indistinguishable from NREM sleep, with EEG power decreasing gradually in parallel with decreasing body temperature. Furthermore, during deep hypothermia REM sleep was largely abolished, but we observed brief and intense bursts of muscle activity, which resembled the regular motor discharges seen during early ontogeny associated with immature sleep patterns. We conclude that torpor and sleep are electrophysiologically on a continuum, and that, in order for torpor to occur, mice need to first transition through euthermic sleep. 3| P a g e

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Mapping sleep's oscillatory events as a biomarker of Alzheimer's disease

Pulver,

Kronberg,

Medenblik

et al. 2023

Alzheimer's & Dementia

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INTRODUCTIONMemory‐associated neural circuits produce oscillatory events including theta bursts (TBs), sleep spindles (SPs), and slow waves (SWs) in sleep electroencephalography (EEG). Changes in the “coupling” of these events may indicate early Alzheimer's disease (AD) pathogenesis.METHODSWe analyzed 205 aging adults using single‐channel sleep EEG, cerebrospinal fluid (CSF) AD biomarkers, and Clinical Dementia Rating® (CDR®) scale. We mapped SW‐TB and SW‐SP neural circuit coupling precision to amyloid positivity, cognitive impairment, and CSF AD biomarkers.RESULTSCognitive impairment correlated with lower TB spectral power in SW‐TB coupling. Cognitively unimpaired, amyloid positive individuals demonstrated lower precision in SW‐TB and SW‐SP coupling compared to amyloid negative individuals. Significant biomarker correlations were found in oscillatory event coupling with CSF Aβ42/Aβ40, phosphorylated‐ tau181, and total‐tau.DISCUSSIONSleep‐dependent memory processing integrity in neural circuits can be measured for both SW‐TB and SW‐SP coupling. This breakdown associates with amyloid positivity, increased AD pathology, and cognitive impairment.Highlights At‐home sleep EEG is a potential biomarker of neural circuits linked to memory. Circuit precision is associated with amyloid positivity in asymptomatic aging adults. Levels of CSF amyloid and tau also correlate with circuit precision in sleep EEG. Theta burst EEG power is decreased in very early mild cognitive impairment. This technique may enable inexpensive wearable EEGs for monitoring brain health.

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Oscillating circuitries in the sleeping brain

Cited by 190 publications

References 307 publications

Post-ictal generalized EEG suppression and seizure-induced mortality are reduced by enhancing dorsal raphe serotonergic neurotransmission

Post-ictal generalized EEG suppression and seizure-induced mortality are reduced by enhancing dorsal raphe serotonergic neurotransmission

The relationship between fasting-induced torpor, sleep and wakefulness in the laboratory mouse

Mapping sleep's oscillatory events as a biomarker of Alzheimer's disease

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