scholarly journals Vigilance and behavioral state-dependent modulation of cortical neuronal activity throughout the sleep/wake cycle

2021 ◽  
Author(s):  
Aurelie Brecier ◽  
Melodie Borel ◽  
Nadia Urbain ◽  
Luc J Gentet

GABAergic inhibitory neurons, through their molecular, anatomic and physiological diversity, provide a substrate for the modulation of ongoing cortical circuit activity throughout the sleep-wake cycle. Here, we investigated neuronal activity dynamics of parvalbumin (PV), vasoactive intestinal polypeptide (VIP) and somatostatin (SST) neurons in naturally-sleeping head-restrained mice at the level of layer 2/3 of the primary somatosensory barrel cortex of mice. Through calcium-imaging and targeted single-unit loose-patch or whole-cell recordings, we found that PV action potential (AP) firing activity was largest during both NREM (non-rapid eye movement) and REM sleep stages, that VIP neurons were activated during REM sleep and that the overall activity of SST neurons remained stable throughout the sleep/wake cycle. Analysis of neuronal activity dynamics uncovered rapid decreases in PV cell firing at wake onset followed by a progressive recovery during wake. Simultaneous local field potential (LFP) recordings further revealed that, except for SST neurons, a large proportion of neurons were modulated by ongoing delta and theta waves. During NREM sleep spindles, PV and SST activity increased and decreased, respectively. Finally, we uncovered the presence of whisking behavior in mice during REM sleep and show that the activity of VIP and SST is differentially modulated during awake and sleeping whisking bouts, which may provide a neuronal substrate for internal brain representations occurring during sleep.


Author(s):  
Michelle A. Frazer ◽  
Yesenia Cabrera ◽  
Rockelle S. Guthrie ◽  
Gina R. Poe

Abstract Purpose of review This paper reviews all optogenetic studies that directly test various sleep states, traits, and circuit-level activity profiles for the consolidation of different learning tasks. Recent findings Inhibiting or exciting neurons involved either in the production of sleep states or in the encoding and consolidation of memories reveals sleep states and traits that are essential for memory. REM sleep, NREM sleep, and the N2 transition to REM (characterized by sleep spindles) are integral to memory consolidation. Neural activity during sharp-wave ripples, slow oscillations, theta waves, and spindles are the mediators of this process. Summary These studies lend strong support to the hypothesis that sleep is essential to the consolidation of memories from the hippocampus and the consolidation of motor learning which does not necessarily involve the hippocampus. Future research can further probe the types of memory dependent on sleep-related traits and on the neurotransmitters and neuromodulators required.



SLEEP ◽  
2020 ◽  
Vol 43 (Supplement_1) ◽  
pp. A30-A30
Author(s):  
J Stucynski ◽  
A Schott ◽  
J Baik ◽  
J Hong ◽  
F Weber ◽  
...  

Abstract Introduction The neural circuits controlling rapid eye movement (REM) sleep, and in particular the role of the medulla in regulating this brain state, remains an active area of study. Previous electrophysiological recordings in the dorsomedial medulla (DM) and electrical stimulation experiments suggested an important role of this area in the control of REM sleep. However the identity of the involved neurons and their precise role in REM sleep regulation are still unclear. Methods The properties of DM GAD2 neurons in mice were investigated through stereotaxic injection of CRE-dependent viruses in conjunction with implantation of electrodes for electroencephalogram (EEG) and electromyogram (EMG) recordings and optic fibers. Experiments included in vivo calcium imaging (fiber photometry) across sleep and wake states, optogenetic stimulation of cell bodies, chemogenetic excitation and suppression (DREADDs), and connectivity mapping using viral tracing and optogenetics. Results Imaging the calcium activity of DM GAD2 neurons in vivo indicates that these neurons are most active during REM sleep. Optogenetic stimulation of DM GAD2 neurons reliably triggered transitions into REM sleep from NREM sleep. Consistent with this, chemogenetic activation of DM GAD2 neurons increased the amount of REM sleep while inhibition suppressed its occurrence and enhanced NREM sleep. Anatomical tracing revealed that DM GAD2 neurons project to several areas involved in sleep / wake regulation including the wake-promoting locus coeruleus (LC) and the REM sleep-suppressing ventrolateral periaquaductal gray (vlPAG). Optogenetic activation of axonal projections from DM to LC, and DM to vlPAG was sufficient to induce REM sleep. Conclusion These experiments demonstrate that DM inhibitory neurons expressing GAD2 powerfully promote initiation of REM sleep in mice. These findings further characterize the dorsomedial medulla as a critical structure involved in REM sleep regulation and inform future investigations of the REM sleep circuitry. Support R01 HL149133



2020 ◽  
Author(s):  
Joseph A. Stucynski ◽  
Amanda L. Schott ◽  
Justin Baik ◽  
Shinjae Chung ◽  
Franz Weber

ABSTRACTThe two major stages of mammalian sleep – rapid eye movement sleep (REMs) and non-REM sleep (NREMs) – are characterized by distinct brain rhythms ranging from millisecond to minute-long (infraslow) oscillations. The mechanisms controlling transitions between sleep stages and how they are synchronized with infraslow rhythms remain poorly understood. Using opto- and chemogenetic manipulation, we show that GABAergic neurons in the dorsomedial medulla (dmM) promote the initiation and maintenance of REMs, in part through their projections to the dorsal and median raphe nuclei. Fiber photometry revealed that dmM GABAergic neurons are strongly activated during REMs. During NREMs, their activity fluctuated in close synchrony with infraslow oscillations in the spindle band of the electroencephalogram, and the phase of this rhythm modulated the latency of optogenetically induced REMs episodes. Thus, dmM inhibitory neurons powerfully promote REMs, and their slow activity fluctuations may coordinate transitions from NREMs to REMs with infraslow brain rhythms.



2017 ◽  
Author(s):  
Elizaveta Solomonova ◽  
Simon Dubé ◽  
Cloé Blanchette-Carrière ◽  
Arnaud Samson-Richer ◽  
Michelle Carr ◽  
...  

Study objectives: Rapid eye movement (REM) sleep, non-rapid eye movement (NREM) sleep, and sleep spindles are all implicated in the consolidation of procedural memories. The relative contributions of sleep stages and sleep spindles was previously shown to depend on individual differences in task processing. Experience with Vipassana meditation is one such individual difference that has not been investigated in relation to sleep. Vipassana meditation is a form of mental training that enhances proprioceptive and somatic awareness and alters attentional style. The goal was thus to examine a potential moderating role for Vipassana meditation experience on sleep-dependent procedural memory consolidation.Methods: Groups of Vipassana meditation practitioners (N=20) and matched meditation-naïve controls (N=20) slept for a single daytime nap in the laboratory. Before and after the nap they completed a procedural task on the Wii Fit balance platform.Results: Meditators performed slightly better on the task before the nap, but the two groups improved similarly after sleep. The groups showed different patterns of sleep-dependent procedural memory consolidation: in meditators task learning was negatively correlated with density of fast and positively correlated with density of slow occipital spindles, while in controls task improvement was associated with increases in REM sleep. Meditation practitioners had a lower density of sleep spindles, especially in occipital regions.Conclusions: Results suggest that neuroplastic changes associated with sustained meditation practice may alter overall sleep architecture and reorganize sleep-dependent patterns of memory consolidation. The lower density of spindles in meditators may mean that meditation practice compensates for some of the memory functions of sleep.



2013 ◽  
Vol 36 (6) ◽  
pp. 613-614
Author(s):  
Gaétane Deliens ◽  
Sophie Schwartz ◽  
Philippe Peigneux

AbstractLlewellyn suggests that episodic memories undergo “elaborative encoding” during rapid eye movement (REM) dreams, generating novel associations between recent and remote memories that are then instantiated during non-REM (NREM) sleep. This hypothesis conflicts with our knowledge of the physiology of NREM and then REM sleep stages and their ordered succession. Moreover, associations during sleep might also involve the extraction of hidden patterns rather than de novo associations.



2013 ◽  
pp. 569-575 ◽  
Author(s):  
I. PEREGRIM ◽  
S. GREŠOVÁ ◽  
M. PALLAYOVÁ ◽  
B. L. FULTON ◽  
J. ŠTIMMELOVÁ ◽  
...  

Although it is thought that obstructive sleep apnea (OSA) is worse during rapid eye movement (REM) sleep than in non-REM (NREM) sleep there are some uncertainties, especially about apnoe-hypopnoe-index (AHI). Several studies found no significant difference in AHI between both sleep stages. However, REM sleep is associated more with side sleeping compared to NREM sleep, which suggests that body position is a possible confounding factor. The main purpose of this study was to compare the AHI in REM and NREM sleep in both supine and lateral body position. A retrospective study was performed on 422 consecutive patients who underwent an overnight polysomnography. Women had higher AHI in REM sleep than NREM sleep in both supine (46.05±26.26 vs. 23.91±30.96, P<0.01) and lateral (18.16±27.68 vs. 11.30±21.09, P<0.01) body position. Men had higher AHI in REM sleep than NREM sleep in lateral body position (28.94±28.44 vs. 23.58±27.31, P<0.01), however, they did not reach statistical significance in supine position (49.12±32.03 in REM sleep vs. 45.78±34.02 in NREM sleep, P=0.50). In conclusion, our data suggest that REM sleep is a contributing factor for OSA in women as well as in men, at least in lateral position.



2019 ◽  
Author(s):  
Masako Tamaki ◽  
Zhiyan Wang ◽  
Tyler Barnes-Diana ◽  
Aaron V. Berard ◽  
Edward Walsh ◽  
...  

AbstractSleep is beneficial for learning. However, whether NREM or REM sleep facilitates learning, whether the learning facilitation results from plasticity increases or stabilization and whether the facilitation results from learning-specific processing are all controversial. Here, after training on a visual task we measured the excitatory and inhibitory neurochemical (E/I) balance, an index of plasticity in human visual areas, for the first time, while subjects slept. Off-line performance gains of presleep learning were associated with the E/I balance increase during NREM sleep, which also occurred without presleep training. In contrast, increased stabilization was associated with decreased E/I balance during REM sleep only after presleep training. These indicate that the above-mentioned issues are not matters of controversy but reflect opposite neurochemical processing for different roles in learning during different sleep stages: NREM sleep increases plasticity leading to performance gains independently of learning, while REM sleep decreases plasticity to stabilize learning in a learning-specific manner.



SLEEP ◽  
2021 ◽  
Author(s):  
Raffaele Ferri ◽  
Maria P Mogavero ◽  
Oliviero Bruni ◽  
Giuseppe Plazzi ◽  
Carlos H Schenck ◽  
...  

Abstract Study Objectives To assess if selective serotonin reuptake inhibitor (SSRI) antidepressants are able to modify the chin EMG tone during sleep also in children. Methods Twenty-three children and adolescents (12 girls, mean age 14.1 years, SD 2.94) under therapy with antidepressant for their mood disorder were consecutively recruited and had a PSG recording. Twenty-one were taking were taking SSRI and treatment duration was 2-12 months. An age- and sex matched group of 33 control children (17 girls, mean age 14.2 years, SD 2.83) and 24 children with narcolepsy type 1 (12 girls, mean age 13.7 years, SD 2.80) were also included. The Atonia Index was then computed for each NREM sleep stage and for REM sleep, also all EMG activations were counted. Results Atonia Index in all sleep stages was found to be significantly reduced in children with narcolepsy followed by the group taking SSRI antidepressants and the number of EMG activations was also increased in both groups. Fluoxetine, in particular, was found to be significantly associated with reduced Atonia index during NREM sleep stages N1, N2, and N3, and with increased number of EMG activations/hour during sleep stage N3. Conclusions Similarly to adults, SSRI antidepressants are able to modify the chin EMG tone also in children during REM sleep, as well as during NREM sleep stages. Different pharmacological properties of the different SSRI might explain the differential effect on chin tone during sleep found in this study.



SLEEP ◽  
2020 ◽  
Author(s):  
Shawn D X Kong ◽  
Camilla M Hoyos ◽  
Craig L Phillips ◽  
Andrew C McKinnon ◽  
Pinghsiu Lin ◽  
...  

Abstract Study Objectives Cardiovascular autonomic dysfunction, as measured by short-term diurnal heart rate variability (HRV), has been reported in older adults with mild cognitive impairment (MCI). However, it is unclear whether this impairment also exists during sleep in this group. We, therefore, compared overnight HRV during sleep in older adults with MCI and those with subjective cognitive impairment (SCI). Methods Older adults (n = 210) underwent overnight polysomnography. Eligible participants were characterized as multi-domain MCI or SCI. The multi-domain MCI group was comprised of amnestic and non-amnestic subtypes. Power spectral analysis of HRV was conducted on the overnight electrocardiogram during non-rapid eye movement (NREM), rapid eye movement (REM), N1, N2, N3 sleep stages, and wake periods. High-frequency HRV (HF-HRV) was employed as the primary measure to estimate parasympathetic function. Results The MCI group showed reduced HF-HRV during NREM sleep (p = 0.018), but not during wake or REM sleep (p &gt; 0.05) compared to the SCI group. Participants with aMCI compared to SCI had the most pronounced reduction in HF-HRV across all NREM sleep stages—N1, N2, and N3, but not during wake or REM sleep. The naMCI sub-group did not show any significant differences in HF-HRV during any sleep stage compared to SCI. Conclusions Our study showed that amnestic MCI participants had greater reductions in HF-HRV during NREM sleep, relative to those with SCI, suggesting potential vulnerability to sleep-related parasympathetic dysfunction. HF-HRV, especially during NREM sleep, may be an early biomarker for dementia detection.



2019 ◽  
Author(s):  
Ada Eban-Rothschild ◽  
Jeremy C. Borniger ◽  
Gideon Rothschild ◽  
William J. Giardino ◽  
Joshua G. Morrow ◽  
...  

AbstractDecades of research have implicated the ventral tegmental area (VTA) in motivation, reinforcement learning and reward processing. We and others recently demonstrated that it also serves as an important node in sleep/wake circuitry. Specifically, VTA-dopaminergic neuron activation is sufficient to drive wakefulness and necessary for the maintenance of wakefulness. However, the role of VTA gamma-aminobutyric acid (GABA)-expressing neurons in arousal regulation is not fully understood. It is still unclear whether VTA-GABAergic neurons predictably alter their firing properties across arousal states, what is the nature of interactions between VTA-GABAergic activity and cortical neural oscillations, and how activity in VTA-GABAergic neurons relates to VTA-dopaminergic neurons in the context of sleep/wake regulation. To address these questions, we simultaneously recorded population activity from VTA-GABAergic or VTA-dopaminergic neurons and EEG/EMG signals during spontaneous sleep/wake states and in the presence of salient stimuli in freely-behaving male mice. We observed that VTA-GABAergic neurons exhibit robust arousal-state-dependent alterations in population activity, with high activity and calcium transients during wakefulness and rapid-eye-movement (REM) sleep compared to non-REM (NREM) sleep. During wakefulness, population activity of VTA-GABAergic neurons, but not VTA-dopaminergic neurons, was positively correlated with EEG gamma power and negatively correlated with EEG theta power. During NREM sleep, population activity in both VTA-GABAergic and VTA-dopaminergic neurons negatively correlated with delta, theta, and sigma EEG power bands. Salient stimuli, with both positive and negative valence, activated VTA-GABAergic neurons. The strongest activation was observed for social stimuli irrespective of valence. Together, our data indicate that VTA-GABAergic neurons, like their dopaminergic counterparts, drastically alter their activity across sleep-wake states. Changes in their activity predicts cortical oscillatory patterns reflected in the EEG, which are distinct from EEG spectra associated with dopaminergic neural activity.Statement of SignificanceLittle is known about how ventral tegmental area (VTA) neural ensembles couple arousal to motivated behaviors. Using cell-type specific genetic tools, we investigated the population activity of GABAergic and dopaminergic neurons within the VTA across sleep/wake states and in the presence of salient stimuli. We demonstrate that coordinated neural activity within VTA-GABAergic neurons peaks during wakefulness and REM sleep. Furthermore, neuronal activity in VTA-GABAergic neurons is correlated with high frequency, low amplitude cortical oscillations during waking, but negatively correlated with high amplitude slower frequency oscillations during NREM sleep. Our results demonstrate that VTA-GABAergic neuronal activity is tightly linked to cortical arousal and highlight this population as a potential important node in sleep/wake regulation.



Sign in / Sign up

Export Citation Format

Share Document