Differential Effects on Fast and Slow Spindle Activity, and the Sleep Slow Oscillation in Humans with Carbamazepine and Flunarizine to Antagonize Voltage-Dependent Na+ and Ca2+ Channel Activity

Ayoub, Amr; Aumann, Dominic; Hörschelmann, Anne; Kouchekmanesch, Atossa; Paul, Pia; Born, Jan; Marshall, Lisa

doi:10.5665/sleep.2722

Cited by 90 publications

(85 citation statements)

References 56 publications

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“…The first gradient has been well reported in the scalp literature, with a major distinction drawn between fast/parietal and slow/frontal spindles (Mölle et al, 2011; Mölle et al, 2002; Werth et al, 1997), indicating a strong agreement between the EEG literature in healthy participants and the findings in the current ECoG study in patients with epilepsy. Intriguingly, we find that the transition between fast and slow spindles seems to follow a linear pattern over the parietal and frontal regions, in agreement with previous work (Peter-Derex et al, 2012), instead of a clear dichotomy between fast and slow spindles (Andrillon et al, 2011; Ayoub et al, 2013). …”

Section: Discussionsupporting

confidence: 92%

Spatiotemporal characteristics of sleep spindles depend on cortical location

2017

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Since their discovery almost one century ago, sleep spindles, 0.5–2 s long bursts of oscillatory activity at 9–16 Hz during NREM sleep, have been thought to be global and relatively uniform throughout the cortex. Recent work, however, has brought this concept into question but it remains unclear to what degree spindles are global or local and if their properties are uniform or location-dependent. We addressed this question by recording sleep in eight patients undergoing evaluation for epilepsy with intracranial electrocorticography, which combines high spatial resolution with extensive cortical coverage. We find that spindle characteristics are not uniform but are strongly influenced by the underlying cortical regions, particularly for spindle density and fundamental frequency. We observe both highly isolated and spatially distributed spindles, but in highly skewed proportions: while most spindles are restricted to one or very few recording channels at any given time, there are spindles that occur over widespread areas, often involving lateral prefrontal cortices and superior temporal gyri. Their co-occurrence is affected by a subtle but significant propagation of spindles from the superior prefrontal regions and the temporal cortices towards the orbitofrontal cortex. This work provides a brain-wide characterization of sleep spindles as mostly local graphoelements with heterogeneous characteristics that depend on the underlying cortical area. We propose that the combination of local characteristics and global organization reflects the dual properties of the thalamo-cortical generators and provides a flexible framework to support the many functions ascribed to sleep in general and spindles specifically.

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Section: Discussionsupporting

confidence: 92%

Spatiotemporal characteristics of sleep spindles depend on cortical location

2017

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“…Can the two types be directly and selectively manipulated based on their different pharmacological profile, as indicated by studies in humans [129] and animal models [50]? Do the similarities between slow spindles and α rhythms (~8-13 Hz) in humans and primates, typical for quiet wakefulness [130], reflect common generating mechanisms and functions?…”

Section: Box 3 Outstanding Questionsmentioning

confidence: 99%

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Astori

Wimmer²,

Lüthi³

2013

Trends in Neurosciences

127

113

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Abstract:Sleep spindles are distinctive electroencephalographic (EEG) oscillations emerging during non-rapid-eye-movement sleep (NREMS) that have been implicated in multiple brain functions, including sleep quality, sensory gating, learning and memory. Despite considerable knowledge about the mechanisms underlying these neuronal rhythms, their function remains poorly understood and current views are largely based on correlational evidence. Here, we review recent studies in humans and rodents that have begun to broaden our understanding of the role of spindles in the normal and disordered brain. We show that newly identified molecular substrates of spindle oscillations, in combination with evolving technological progress, offer novel targets and tools to selectively manipulate spindles and dissect their role in sleep-dependent processes. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems CorporationAstori et al. Highlights Newly recognized ion channel subtypes generating spindle rhythms are described. The contribution of spindles to arousal threshold and sleep quality is discussed. The proposed role of spindles in memory consolidation is examined. A function of thalamic spindles in neural development is suggested. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 4 Previous excellent reviews have thoroughly described cellular and network bases of spindle generation [3,6,7]. Here, we first review recent work on genetic models that has expanded the mechanistic understanding of this EEG rhythm through the modification of novel molecular substrates. We then discuss the current views about the functional aspects of spindles in brain physiology and pathology, as obtained from studies in naturally sleeping animals and humans. We highlight studies indicating that spindles are accessible for selective interventions, and that, with emerging technologies, will open avenues to decipher spindle function. Novel molecular aspects of spindle generationSleep spindles emerge from a limited set of cellular participants: the resonating core of these waxing-and-waning oscillations resides in the nRt-TC loop, which sustains repetitive burst discharges of its cellular components under the control of cortical inputs (Figure 1 Another important factor in the generation and maintenance of reticular intrinsic oscillations is the aforementioned SK2 or Kcnn2 channel. The vigorous Ca 2+ influx in nRt dendrites originating from Ca V 3.3 channels gates SK2 channels, thereby creating a burstafterhyperpolarization (bAHP) [12,19]. As T channels recover partially from inactivation duri...

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“…Therefore, it has been suggested that slow and fast spindles may reflect independent mechanisms that contribute to consolidation processing (Molle et al, 2011; Schabus et al, 2007). Furthermore, it has been demonstrated that certain pharmacological interventions can jointly increase slow-spindle activity and slow-oscillatory activity, while simultaneously decreasing fast-spindle activity (Ayoub et al, 2013). Thus, one highly speculative possibility is that by enhancing slow-oscillatory activity with SOS in elderly adults, a concomitant decrease in fast-spindle activity might be produced, but further research is necessary to assess this possibility.…”

Section: Discussionmentioning

confidence: 99%

Memory improvement via slow-oscillatory stimulation during sleep in older adults

Westerberg

Florczak

Weıntraub

et al. 2015

Neurobiology of Aging

Self Cite

139

125

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We examined the intriguing but controversial idea that disrupted sleep-dependent consolidation contributes to age-related memory decline. Slow-wave activity during sleep may help strengthen neural connections and provide memories with long-term stability, in which case decreased slow-wave activity in older adults could contribute to their weaker memories. One prediction from this account is that age-related memory deficits should be reduced by artificially enhancing slow-wave activity. In young adults, applying transcranial current oscillating at a slow frequency (.75 Hz) during sleep improves memory. Here, we tested whether this procedure can improve memory in older adults. In two sessions separated by 1 week, we applied either slow-oscillatory stimulation or sham stimulation during an afternoon nap in a double-blind, crossover design. Memory tests were administered before and after sleep. A larger improvement in word-pair recall and higher slow-wave activity were observed with slow-oscillatory stimulation than with sham stimulation. This is the first demonstration that this procedure can improve memory in older adults, suggesting that declarative memory performance in older adults is partly dependent on slow-wave activity during sleep.

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Differential Effects on Fast and Slow Spindle Activity, and the Sleep Slow Oscillation in Humans with Carbamazepine and Flunarizine to Antagonize Voltage-Dependent Na+ and Ca2+ Channel Activity

Cited by 90 publications

References 56 publications

Spatiotemporal characteristics of sleep spindles depend on cortical location

Spatiotemporal characteristics of sleep spindles depend on cortical location

Manipulating sleep spindles – expanding views on sleep, memory, and disease

Memory improvement via slow-oscillatory stimulation during sleep in older adults

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