Author response: Propagated infra-slow intrinsic brain activity reorganizes across wake and slow wave sleep

Propagation of slow intrinsic brain activity has been widely observed in electrophysiogical studies of slow wave sleep (SWS). However, in human resting state fMRI (rs-fMRI), intrinsic activity has been understood predominantly in terms of zero-lag temporal synchrony (functional connectivity) within systems known as resting state networks (RSNs). Prior rs-fMRI studies have found that RSNs are generally preserved across wake and sleep. Here, we use a recently developed analysis technique to study propagation of infra-slow intrinsic blood oxygen level dependent (BOLD) signals in normal adults during wake and SWS. This analysis reveals marked changes in propagation patterns in SWS vs. wake. Broadly, ordered propagation is preserved within traditionally defined RSNs but lost between RSNs. Additionally, propagation between cerebral cortex and subcortical structures reverses directions, and intra-cortical propagation becomes reorganized, especially in visual and sensorimotor cortices. These findings show that propagated rs-fMRI activity informs theoretical accounts of the neural functions of sleep.

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Selection of stimulus parameters for enhancing slow wave sleep events with a Neural-field theory thalamocortical computational model

10.1101/2021.02.03.429528 ◽

2021 ◽

Author(s):

Felipe A. Torres ◽

Patricio Orio ◽

María-José Escobar

Keyword(s):

Computational Model ◽

Slow Wave ◽

Memory Consolidation ◽

Closed Loop ◽

Slow Wave Sleep ◽

Brain Activity ◽

Sensory Stimulation ◽

Sleep Spindles ◽

Slow Oscillations ◽

Closed Loop Stimulation

AbstractSlow-wave sleep cortical brain activity, conformed by slow-oscillations and sleep spindles, plays a key role in memory consolidation. The increase of the power of the slow-wave events, obtained by auditory sensory stimulation, positively correlates to memory consolidation performance. However, little is known about the experimental protocol maximizing this effect, which could be induced by the power of slow-oscillation, the number of sleep spindles, or the timing of both events’ co-occurrence. Using a mean-field model of thalamocortical activity, we studied the effect of several stimulation protocols, varying the pulse shape, duration, amplitude, and frequency, as well as a target-phase using a closed-loop approach. We evaluated the effect of these parameters on slow-oscillations (SO) and sleep-spindles (SP), considering: (i) the power at the frequency bands of interest, (ii) the number of SO and SP, (iii) co-occurrences between SO and SP, and (iv) synchronization of SP with the up-peak of the SO. The first three targets are maximized using a decreasing ramp pulse with a pulse duration of 50 ms. Also, we observed a reduction in the number of SO when increasing the stimulus energy by rising its amplitude. To assess the target-phase parameter, we applied closed-loop stimulation at 0º, 45º, and 90º of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0º stimulation produces better results in the power and number of SO and SP than the rhythmic or aleatory stimulation. On the other hand, stimulating at 45º or 90º change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0º phase. Finally, we propose the application of closed-loop stimulation at the rising zero-cross point using pulses with a decreasing ramp shape and 50 ms of duration for future experimental work.Author summaryDuring the non-REM (NREM) phase of sleep, events that are known as slow oscillations (SO) and spindles (SP) can be detected by EEG. These events have been associated with the consolidation of declarative memories and learning. Thus, there is an ongoing interest in promoting them during sleep by non-invasive manipulations such as sensory stimulation. In this paper, we used a computational model of brain activity that generates SO and SP, to investigate which type of sensory stimulus –shape, amplitude, duration, periodicity– would be optimal for increasing the events’ frequency and their co-occurrence. We found that a decreasing ramp of 50 ms duration is the most effective. The effectiveness increases when the stimulus pulse is delivered in a closed-loop configuration triggering the pulse at a target phase of the ongoing SO activity. A desirable secondary effect is to promote SPs at the rising phase of the SO oscillation.

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0078 Influence of Light on Brain Activity Upon Waking From Slow Wave Sleep

SLEEP ◽

10.1093/sleep/zsaa056.076 ◽

2020 ◽

Vol 43 (Supplement_1) ◽

pp. A31-A32 ◽

Cited By ~ 1

Author(s):

E E Flynn-Evans ◽

C J Hilditch ◽

R Chachad ◽

K Bansal ◽

L R Wong ◽

...

Keyword(s):

Slow Wave ◽

Slow Wave Sleep ◽

Brain Activity ◽

Effective Connectivity ◽

Red Light ◽

Spectral Composition ◽

Brain Regions ◽

Graphical Analysis ◽

Sleep Inertia ◽

Temporal Persistence

Abstract Introduction Waking from sleep is associated with reduced alertness due to sleep inertia. Light acutely improves alertness during sleep deprivation. In this study we assessed the influence of light on brain activity and connectivity after waking from slow wave sleep (SWS). Methods Twelve participants kept an actigraphy-confirmed stable sleep schedule with 8.5 hours for five nights and five hours for one night prior to an overnight laboratory visit. Participants completed two three-minute Karolinska Drowsiness Tests (KDT) before going to bed at their habitual bedtime. They were monitored continuously using high-density EEG (32-channel; Brain Products GmbH). Participants were woken twice and exposed to red light (0.01 melanopic-lux; control) or blue-enriched light (63.62 melanopic-lux) for one hour, in a randomized order, following at least five minutes of SWS. EEG artifact were removed algorithmically and the spectral composition of each electrode (i.e., fast fourier transform, FFT) and effective connectivity (i.e., partial directed coherence, PDC) between each electrode were estimated. A graphical analysis was conducted to extract features relevant to the facilitation of efficient communication between electrodes. All data were averaged within frequency bins of interest that correspond to delta (1-3Hz), theta (4-7Hz), alpha (8-12Hz), and beta (13-25Hz) bands and expressed relative to the pre-sleep baseline. Results Compared to the pre-sleep baseline, participants exposed to blue-enriched light experienced reduced theta and alpha activity; however, these results were not significantly different from the control. In contrast, the communication of frontal electrodes significantly increased across all frequency bands compared to the control, and this effect was most prominent in the alpha (t(11)=3.80, p=.005) and beta bands (t(11)=3.92, p=.004). Conclusion Exposure to blue-enriched light immediately after waking from SWS may accelerate the process of waking and help to improve alertness by facilitating communication between brain regions. Future analyses will explore the temporal persistence and granularity of the communicative properties associated with this response. Support Naval Postgraduate School Grant. NASA Airspace Operations and Safety Program, System-Wide Safety Project.

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Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2010.2316 ◽

2011 ◽

Vol 278 (1717) ◽

pp. 2419-2428 ◽

Cited By ~ 72

Author(s):

John A. Lesku ◽

Alexei L. Vyssotski ◽

Dolores Martinez-Gonzalez ◽

Christiane Wilzeck ◽

Niels C. Rattenborg

Keyword(s):

Slow Wave ◽

Rem Sleep ◽

Visual Processing ◽

Slow Wave Sleep ◽

Brain Activity ◽

Brain Regions ◽

Avian Brain ◽

Brain Functioning ◽

Sleep Homeostasis ◽

Local Sleep

The function of the brain activity that defines slow wave sleep (SWS) and rapid eye movement (REM) sleep in mammals is unknown. During SWS, the level of electroencephalogram slow wave activity (SWA or 0.5–4.5 Hz power density) increases and decreases as a function of prior time spent awake and asleep, respectively. Such dynamics occur in response to waking brain use, as SWA increases locally in brain regions used more extensively during prior wakefulness. Thus, SWA is thought to reflect homeostatically regulated processes potentially tied to maintaining optimal brain functioning. Interestingly, birds also engage in SWS and REM sleep, a similarity that arose via convergent evolution, as sleeping reptiles and amphibians do not show similar brain activity. Although birds deprived of sleep show global increases in SWA during subsequent sleep, it is unclear whether avian sleep is likewise regulated locally. Here, we provide, to our knowledge, the first electrophysiological evidence for local sleep homeostasis in the avian brain. After staying awake watching David Attenborough's The Life of Birds with only one eye, SWA and the slope of slow waves (a purported marker of synaptic strength) increased only in the hyperpallium—a primary visual processing region—neurologically connected to the stimulated eye. Asymmetries were specific to the hyperpallium, as the non-visual mesopallium showed a symmetric increase in SWA and wave slope. Thus, hypotheses for the function of mammalian SWS that rely on local sleep homeostasis may apply also to birds.

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Selection of stimulus parameters for enhancing slow wave sleep events with a neural-field theory thalamocortical model

PLoS Computational Biology ◽

10.1371/journal.pcbi.1008758 ◽

2021 ◽

Vol 17 (7) ◽

pp. e1008758

Author(s):

Felipe A. Torres ◽

Patricio Orio ◽

María-José Escobar

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Closed Loop ◽

Slow Wave Sleep ◽

Brain Activity ◽

Sleep Spindles ◽

Mean Field Model ◽

Cross Point ◽

Slow Oscillations ◽

Closed Loop Stimulation

Slow-wave sleep cortical brain activity, conformed by slow-oscillations and sleep spindles, plays a key role in memory consolidation. The increase of the power of the slow-wave events, obtained by auditory sensory stimulation, positively correlates to memory consolidation performance. However, little is known about the experimental protocol maximizing this effect, which could be induced by the power of slow-oscillation, the number of sleep spindles, or the timing of both events’ co-occurrence. Using a mean-field model of thalamocortical activity, we studied the effect of several stimulation protocols, varying the pulse shape, duration, amplitude, and frequency, as well as a target-phase using a closed-loop approach. We evaluated the effect of these parameters on slow-oscillations (SO) and sleep-spindles (SP), considering: (i) the power at the frequency bands of interest, (ii) the number of SO and SP, (iii) co-occurrences between SO and SP, and (iv) synchronization of SP with the up-peak of the SO. The first three targets are maximized using a decreasing ramp pulse with a pulse duration of 50 ms. Also, we observed a reduction in the number of SO when increasing the stimulus energy by rising its amplitude. To assess the target-phase parameter, we applied closed-loop stimulation at 0°, 45°, and 90° of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0° stimulation produces better results in the power and number of SO and SP than the rhythmic or random stimulation. On the other hand, stimulating at 45° or 90° change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0° phase. Finally, we propose the application of closed-loop stimulation at the rising zero-cross point using pulses with a decreasing ramp shape and 50 ms of duration for future experimental work.

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Reward biases spontaneous neural reactivation during sleep

Nature Communications ◽

10.1038/s41467-021-24357-5 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Virginie Sterpenich ◽

Mojca K. M. van Schie ◽

Maximilien Catsiyannis ◽

Avinash Ramyead ◽

Stephen Perrig ◽

...

Keyword(s):

Functional Mri ◽

Slow Wave ◽

Slow Wave Sleep ◽

Life Experiences ◽

Brain Activity ◽

Memory Performance ◽

Neural Mechanism ◽

Brain Regions ◽

Evolutionary Perspective ◽

Neural Representations

AbstractSleep favors the reactivation and consolidation of newly acquired memories. Yet, how our brain selects the noteworthy information to be reprocessed during sleep remains largely unknown. From an evolutionary perspective, individuals must retain information that promotes survival, such as avoiding dangers, finding food, or obtaining praise or money. Here, we test whether neural representations of rewarded (compared to non-rewarded) events have priority for reactivation during sleep. Using functional MRI and a brain decoding approach, we show that patterns of brain activity observed during waking behavior spontaneously reemerge during slow-wave sleep. Critically, we report a privileged reactivation of neural patterns previously associated with a rewarded task (i.e., winning at a complex game). Moreover, during sleep, activity in task-related brain regions correlates with better subsequent memory performance. Our study uncovers a neural mechanism whereby rewarded life experiences are preferentially replayed and consolidated while we sleep.

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Modal-Polar Representation of Evoked Response Potentials in Multiple Arousal States

Frontiers in Human Neuroscience ◽

10.3389/fnhum.2021.642479 ◽

2021 ◽

Vol 15 ◽

Author(s):

Rawan K. El-Zghir ◽

Natasha C. Gabay ◽

Peter A. Robinson

Keyword(s):

Transfer Function ◽

Slow Wave ◽

Slow Wave Sleep ◽

Brain Activity ◽

Evoked Response ◽

Temporal Part ◽

Sleep State ◽

Global Mode ◽

Eyes Closed ◽

Evoked Response Potentials

An expansion of the corticothalamic transfer function into eigenmodes and resonant poles is used to derive a simple formula for evoked response potentials (ERPs) in various states of arousal. The transfer function corresponds to the cortical response to an external stimulus, which encodes all the information and properties of the linear system. This approach links experimental observations of resonances and characteristic timescales in brain activity with physically based neural field theory (NFT). The present work greatly simplifies the formula of the analytical ERP, and separates its spatial part (eigenmodes) from the temporal part (poles). Within this framework, calculations involve contour integrations that yield an explicit expression for ERPs. The dominant global mode is considered explicitly in more detail to study how the ERP varies with time in this mode and to illustrate the method. For each arousal state in sleep and wake, the resonances of the system are determined and it is found that five poles are sufficient to study the main dynamics of the system in waking eyes-open and eyes-closed states. Similarly, it is shown that six poles suffice to reproduce ERPs in rapid-eye movement sleep, sleep state 1, and sleep state 2 states, whereas just four poles suffice to reproduce the dynamics in slow wave sleep. Thus, six poles are sufficient to preserve the main global ERP dynamics of the system for all states of arousal. These six poles correspond to the dominant resonances of the system at slow-wave, alpha, and beta frequencies. These results provide the basis for simplified analytic treatment of brain dynamics and link observations more closely to theory.

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