Coordinated infraslow neural and cardiac oscillations mark fragility and offline periods in mammalian sleep

Lecci, Sandro; Fernandez, Laura M. J.; Weber, Frederik D.; Cardis, Romain; Chatton, Jean–Yves; Born, Jan; Lüthi, Anita

doi:10.1126/sciadv.1602026

Cited by 178 publications

(339 citation statements)

References 54 publications

(81 reference statements)

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“…At ISL>5 s, the reduced spindle likelihood (right side of Fig 2F) may reflect the initial shift to a sleep state not conducive to spindles. Additionally, we found a strong peak at an infraslow frequency (~0.02 Hz; Fig 2B), in line with a recent report suggesting the presence of spindle-rich intervals separated by ~50 s (27). Our findings therefore underscore the importance of considering spindles on the meso-scale (~0.2-0.3 Hz), intermediate between the sub-second scale of the oscillations themselves (11)(12)(13)(14)(15)(16) and the infra-slow scale just under a minute (0.02 Hz).…”

supporting

confidence: 93%

Sleep spindle refractoriness segregates periods of memory reactivation

Antony

Piloto

Wang

et al. 2017

Preprint

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Abstract:The stability of long-term memories is enhanced by reactivation during sleep. Correlative evidence has linked memory reactivation with thalamocortical sleep spindles, although their functional role is poorly understood. Our initial study replicated this correlation but also demonstrated a novel rhythmicity to spindles, such that spindles are less likely to occur immediately following other spindles. We leveraged this rhythmicity to test the role of spindles in memory by using real-time spindle tracking to present cues inside versus outside the presumptive refractory period; as predicted, cues presented outside the refractory period led to better memory. Our findings reveal a previously undescribed neural mechanism whereby spindles segment sleep into two distinct substates: prime opportunities for reactivation and gaps that segregate reactivation events. One Sentence Summary:The characteristic timing of sleep spindles regulates when memories can be reactivated during sleep. Main Text:Memories of daytime episodes are covertly reactivated during sleep, improving memory storage in the brain (1). Previous research has implicated three electrophysiological signals in memory processing during sleep. The slowest of these are sleep slow oscillations (SOs), brain rhythms at approximately 1 Hz prominent during deep sleep (2). A second signal is the sleep spindle, a burst of activity at 11-16 Hz lasting 0.5-3 s. Third, replay of newly formed memories is thought to occur in conjunction with high-frequency bursts of hippocampal and cortical activity called ripples (1,3,4). These three signals can occur with precise temporal interrelationships; spindles tend to occur most often during the up-state phase of SOs, and ripples tend to occur at spindle troughs (5-7). To the extent that these relationships are evidenced, memory consolidation appears to be more effective (8), suggesting a dual cross-frequency coupling mechanism by which initially hippocampal-dependent memories become stabilized in long-term neocortical networks over time (2). Pharmacological evidence suggests spindles promote memory consolidation in humans (9); however, the time course relating spindles to memory consolidation has not been well-characterized.Here, we investigated and manipulated temporal relationships between spindles and learningrelated auditory cues known to boost memory, relying on a technique called targeted memory reactivation (TMR) (10,11). In experiment 1 (N = 18; Fig 1A), subjects first over-learned novel associations between individual sounds and picture items (e.g., [meow]-Brad Pitt, [violin]-Eiffel Tower). Next, they learned unique locations for each item on a background grid. After an initial test, they took an afternoon nap with background white noise (~40 dB; Table S1 provides sleep stage information). Upon online indications of slow-wave sleep (SWS), we embedded half of the . CC-BY 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not ....

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confidence: 93%

Sleep spindle refractoriness segregates periods of memory reactivation

Antony

Piloto

Wang

et al. 2017

Preprint

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“…However, the average duration of SWA reactivation in CAP was reported as 12.66 s which is longer than our ACE observations. Lecci et al 34 found periodic sigma activity (but not SWA) that was more prevalent in Stage 2 sleep than SWS and associated with memory consolidation in a declarative task (human) as well as hippocampal ripple activity (in mice). The present results, on the other hand, identified a heretofore undescribed burst in HR activity, that correlated with prominent, aperiodic, ACE-related increases in SWA and sigma, as well as parasympathetic activity, that predicted gains in declarative memory during Stage 2 and SWS.…”

Section: Discussionmentioning

confidence: 99%

Coupling of autonomic and central events during sleep benefits declarative memory consolidation

Naji

McDevitt

Bazhenov

et al. 2017

Preprint

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While anatomical pathways between forebrain cognitive and brainstem autonomic nervous centers are well defined, autonomic-central interactions during sleep and their contribution to waking performance are not understood. Here, we analyzed simultaneous central activity via electroencephalography (EEG) and autonomic heart beat-to-beat intervals (RR intervals) from electrocardiography (ECG) during wake and daytime sleep. We identified bursts of ECG activity that lasted 4-5 seconds and predominated in non-rapid-eye-movement sleep (NREM). Using event-based analysis of NREM sleep, we found an increase in delta (0.5-4Hz) and sigma (12-15Hz) power and an elevated density of slow oscillations (0.5-1Hz) about 5 secs prior to peak of the heart rate burst, as well as a surge in vagal activity, assessed by high-frequency (HF) component of RR intervals. Using regression framework, we show that these Autonomic/Central Events (ACE) positively predicted post-nap improvement in a declarative memory task after controlling for the effects of spindles and slow oscillations from sleep periods without ACE. No such relation was found between memory performance and a control nap. Additionally, NREM ACE negatively correlated with REM sleep and learning in a non-declarative memory task. These results provide the first evidence that coordinated autonomic and central events play a significant role in declarative memory consolidation.

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“…However, several neural processes occur over much longer timescales (Huk et al, 2018). Transitions between sleep and wakefulness and between different stages of sleep occur on timescales of minutes and hours (Weber and Dan, 2016;Lecci et al, 2017;Meisel et al, 2017). During wakefulness, changes in arousal can span tens of seconds and minutes, yet they affect performance in sub-second behavioural tasks (Harris and Thiele, 2011;Palva and Palva, 2012;McGinley et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Distinct structure of cortical population activity on fast and infraslow timescales

Okun

Steinmetz

Lak

et al. 2018

Preprint

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Cortical activity is organised across multiple spatial and temporal scales. Most research on the dynamics of neuronal spiking is concerned with timescales of 1 ms ̶ 1 s, and little is known about spiking dynamics on timescales of tens of seconds and minutes. Here, we used frequency domain analyses to study the structure of individual neurons' spiking activity and its coupling to local population rate and to arousal level across frequencies ranging from 0.01 to 100 Hz. In mouse medial prefrontal cortex (mPFC), the spiking dynamics of individual neurons could be quantitatively captured by a combination of interspike interval and firing rate power spectrum distributions. The relative strength of coherence with local population often differed across timescales: a neuron strongly coupled to population rate on fast timescales could be weakly coupled on slow timescales, and vice versa. On slow but not fast timescales, a substantial proportion of neurons showed firing anti-correlated with the population. Infraslow firing rate changes were largely determined by arousal rather than by local factors, which could explain the timescale dependence of population coupling strength of individual neurons. These observations demonstrate how individual neurons simultaneously partake in fast local dynamics, and slow brain-wide dynamics, extending our understanding of infraslow cortical activity beyond the mesoscale resolution of fMRI studies.

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Coordinated infraslow neural and cardiac oscillations mark fragility and offline periods in mammalian sleep

Abstract: Mammalian sleep alternates between sensory-responsive and protected offline periods via coordinated neural and cardiac rhythms.

Cited by 178 publications

References 54 publications

Sleep spindle refractoriness segregates periods of memory reactivation

Sleep spindle refractoriness segregates periods of memory reactivation

Coupling of autonomic and central events during sleep benefits declarative memory consolidation

Distinct structure of cortical population activity on fast and infraslow timescales

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