Local hippocampal fast gamma rhythms precede brain-wide hyperemic patterns during spontaneous rodent REM sleep

Bergel, Antoine; Thomas, Daniel; Demené, Charlie; Tanter, Mickaël; Cohen, Ivan

doi:10.1038/s41467-018-07752-3

Cited by 95 publications

(83 citation statements)

References 48 publications

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“…Since, electrophysiological techniques, such as MEG and EEG, do not rely on neurovascular coupling, they provide a more direct measurement of neural activity without fMRI's susceptibility to respiratory artefacts. Indeed, studies employing electrophysiology in tandem with fMRI have provided many cases in point where BOLD global signal dynamics vary together with neural activity as indexed by local field potentials (Scholvinck et al, 2010;Wong et al, 2013;Liu et al, 2015;Chang et al, 2016;Bergel et al, 2018).…”

Section: Spatial Distribution Of Time Of Day Effectsmentioning

confidence: 99%

“…In another study, Liu and colleagues found that global peaks observed in fMRI signal were associated with spectral shifts in LFP in macaques, and that peaks defined in the same manner exhibited a visual-sensorimotor co-activation pattern in humans (Liu et al, 2018). More recently, Bergel and colleagues used ultrasound imaging in rats to show that brain wide vascular surges lasting between 5 to 30 seconds during REM sleep were preceded by sustained activity in the theta, mid-gamma, and high-gamma LFP bands (Bergel et al, 2018). Importantly, Turchi and colleagues demonstrated that pharmacological inactivation of basal forebrain nuclei selectively decreased global fMRI signal fluctuation ipsilaterally to the injection site even after statistically accounting for end-tidal pCO 2 fluctuation and subject motion (Turchi et al, 2018).…”

Section: Spatial Distribution Of Time Of Day Effectsmentioning

confidence: 99%

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Time of day is associated with paradoxical reductions in global signal fluctuation and functional connectivity

Orban

Kong

et al. 2019

Preprint

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The brain exhibits substantial diurnal variation in physiology and function but neuroscience studies rarely report or consider the effects of time of day. Here, we examined variation in resting-state fMRI in around 900 subjects scanned between 8am to 10pm on two different days. Multiple studies across animals and humans have demonstrated that the brain's global signal amplitude (henceforth referred to as "fluctuation") increases with decreased arousal.Thus, in accord with known circadian variation in arousal, we hypothesised that global signal fluctuation would be lowest in the morning, increase in the mid-afternoon and dip in the early evening. Instead, we observed a cumulative decrease (22% between 9am to 9pm) in global signal fluctuation as the day progressed. To put the magnitude of this decrease in context, we note that task-evoked fMRI responses are typically in the order of 1% to 3%. Respiratory variation also decreased with time of day, although control analyses suggested that this did not account for the reduction in GS fluctuation. Finally, time of day was associated with marked decreases in resting state functional connectivity across the whole brain. The magnitude of decrease was significantly stronger than associations between functional connectivity and behaviour (e.g., fluid intelligence). These findings reveal unexpected effects of time of day on the resting human brain, which challenge the prevailing notion that the brain's global signal reflects mostly arousal and physiological artefacts. We conclude by discussing potential mechanisms for the observed diurnal variation in resting brain activity and the importance of accounting for time of day in future studies.

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Section: Spatial Distribution Of Time Of Day Effectsmentioning

confidence: 99%

Section: Spatial Distribution Of Time Of Day Effectsmentioning

confidence: 99%

Time of day is associated with paradoxical reductions in global signal fluctuation and functional connectivity

Orban

Kong

et al. 2019

Preprint

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“…phase-locked activity with fast gamma (80-110 Hz) in the hippocampus may relate to the recent 376 observation that demonstrated the close association between local hippocampal theta and fast 377 gamma events and brain-wide hyperemic events (Bergel et al, 2018). Because a number of 378 hippocampal neurons fire immediately after P-waves ( Fig.…”

Section: State-dependent Global Coordination Of Neural Ensembles 373mentioning

confidence: 87%

State-dependent pontine ensemble dynamics and interactions with cortex across sleep states

Tsunematsu

Patel

Onken

et al. 2019

Preprint

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15The pontine nuclei play a crucial role in sleep-wake regulation. However, pontine ensemble 16 dynamics underlying sleep regulation remain poorly understood. By monitoring population 17 activity in multiple pontine and adjacent brainstem areas, here we show slow, state-predictive 18 pontine ensemble dynamics and state-dependent interactions between the pons and the 19 cortex in mice. On a timescale of seconds to minutes, pontine populations exhibit diverse 20 firing across vigilance states, with some of these dynamics being attributed to cell type-21 specific activity. Pontine population activity can predict pupil dilation and vigilance states: 22 pontine neurons exhibit longer predictable power compared with hippocampal neurons. On 23 a timescale of sub-seconds, pontine waves (P-waves) are observed as synchronous firing of 24 pontine neurons primarily during rapid eye movement (REM) sleep, but also during non-REM 25 (NREM) sleep. Crucially, P-waves functionally interact with cortical activity in a state-26 dependent manner: during NREM sleep, hippocampal sharp wave-ripples (SWRs) precede P-27 waves. On the other hand, P-waves during REM sleep are phase-locked with ongoing 28 hippocampal theta oscillations and are followed by burst firing in a subset of hippocampal 29 neurons. Thus, the directionality of functional interactions between the hippocampus and 30 pons changes depending on sleep states. This state-dependent global coordination between 31 pontine and cortical regions implicates distinct functional roles of sleep. 32 33 Keywords 34 brainstem, brain state, sleep, neural ensemble dynamics, neural oscillations, P/PGO waves 35

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“…The variability in results between groups may be influenced by anesthesia type and levels, both of which have large effects on the amplitude of the arterial dilations elicited during functional hyperemia 34 . Finally, brain-wide hyperemia observed during sleep 67 can explain improved tracer transport in the brain observed during sleep 59 .…”

Section: Discussionmentioning

confidence: 98%

Functional hyperemia drives fluid exchange in the paravascular space

Kedarasetti

Turner

Echagarruga

et al. 2019

Preprint

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Maintaining the ionic and chemical composition of the extracellular spaces in the brain is extremely important for its health and function. However, the brain lacks a conventional lymphatic system to remove metabolic waste. It has been proposed that the fluid movement through the paravascular space (PVS) surrounding penetrating arteries can help remove metabolites from the brain. The dynamics of fluid movement in the PVS and its interaction with arterial dilation and brain mechanics are not well understood. Here, we performed simulations to understand how arterial pulsations and dilations interact with brain deformability to drive fluid flow in the PVS. In simulations with compliant brain tissue, arterial pulsations did not drive appreciable flows in the PVS. In contrast, when the artery dilated with dynamics like those seen during functional hyperemia, there was a marked movement of fluid through the PVS. Our simulations suggest that in addition to its other purposes, functional hyperemia may serve to increase fluid exchange between the PVS and the subarachnoid space, improving the clearance of metabolic waste. We measured displacement of the blood vessels and the brain tissue simultaneously in awake, headfixed mice using two-photon microscopy. Our measurements show that brain tissue can deform in response to fluid movement in the PVS, as predicted by simulations. The results from our simulations and experiments show that the deformability of the soft brain tissue needs to be accounted for when studying fluid flow and metabolite transport in the brain.

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Local hippocampal fast gamma rhythms precede brain-wide hyperemic patterns during spontaneous rodent REM sleep

Cited by 95 publications

References 48 publications

Time of day is associated with paradoxical reductions in global signal fluctuation and functional connectivity

Time of day is associated with paradoxical reductions in global signal fluctuation and functional connectivity

State-dependent pontine ensemble dynamics and interactions with cortex across sleep states

Functional hyperemia drives fluid exchange in the paravascular space

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