Corticothalamic Feedback Controls Sleep Spindle Duration In Vivo

Bonjean, Maxime; Baker, Tanya I.; Lemieux, Maxime; Timofeev, Igor; Sejnowski, Terrence J.; Bazhenov, Maxim

doi:10.1523/jneurosci.0077-11.2011

Cited by 177 publications

(197 citation statements)

References 60 publications

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“…Yet, the cortical (blue) feedback is essential to provide synchronization and spatial coherence of spindling over widespread thalamic regions [48]. More recently, a cortical control of intra-and inter-spindle periods has been postulated [128]. Three distinct phases can be distinguished in sleep spindles, as consistently shown by in vivo intracellular recordings.…”

Section: Box 3 Outstanding Questionsmentioning

confidence: 98%

“…The involvement of increased corticothalamic feedback in provoking these paroxysmal oscillations was confirmed in ferrets [125,126]. Subsequent computational work suggested a cortical contribution to spindle termination: asynchronous cortical firing during the waning phase depolarizes TC cells, thereby 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 inactivating T currents [127,128]. A very recent modeling study implements TC matrix and core pathways, equivalent to distributed and focal projections, respectively, to show that global and local spindle detection may result from preferential monitoring of superficial and deeper cortical layer activity, respectively [56].…”

Section: Box 2 Exploring the Mechanisms Of Spindle Generation With Cmentioning

confidence: 99%

“…In vitro work has explained spindle termination with the Ca 2+ -dependent upregulation of a depolarizing I h current in TC cells [124,134], which induces a refractory inter-spindle period. However, recent data based on a computational model of the TC system have highlighted a contribution of corticothalamic inputs [128]; during the waning phase, cortical firing is no longer phase-locked with inhibitory postsynaptic potentials and drives an overall depolarization in TC cells. This prevents deinactivation of T channels, thus impeding rebound bursting.…”

Section: Box 3 Outstanding Questionsmentioning

confidence: 99%

See 2 more Smart Citations

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

Astori

Wimmer²,

Lüthi³

2013

Trends in Neurosciences

132

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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Section: Box 3 Outstanding Questionsmentioning

confidence: 98%

Section: Box 2 Exploring the Mechanisms Of Spindle Generation With Cmentioning

confidence: 99%

Section: Box 3 Outstanding Questionsmentioning

confidence: 99%

See 1 more Smart Citation

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

Astori

Wimmer²,

Lüthi³

2013

Trends in Neurosciences

132

113

View full text Add to dashboard Cite

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“…At the cellular network level, a large body of studies employing multiunit recordings in animals and computational models has shown that spindles reflect oscillatory activity in widespread thalamocortical (TC) circuits. Although the neural circuitry that supports spindle generation is well known (Steriade, 2005) and involves a complex interaction between reticular (RE), TC, and pyramidal cells, more recent experimental evidence (Bonjean et al, 2011) suggests that corticothalamic input initiates spindles by triggering spike bursts in RE thalamic neurons and is maintained by synchronized firing in the RE-TC-RE circuit (Steriade, Nunez, & Amzica, 1993;von Krosigk, Bal, & McCormick, 1993). Spindles are terminated by desynchronization of the interaction between thalamic and cortical neuronal firing.…”

Section: Discussionmentioning

confidence: 99%

Sleep Spindles and Intellectual Ability: Epiphenomenon or Directly Related?

Fang

Sergeeva

Ray

et al. 2017

Journal of Cognitive Neuroscience

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Abstract■ Sleep spindles-short, phasic, oscillatory bursts of activity that characterize non-rapid eye movement sleep-are one of the only electrophysiological oscillations identified as a biological marker of human intelligence (e.g., cognitive abilities commonly assessed using intelligence quotient tests). However, spindles are also important for sleep maintenance and are modulated by circadian factors. Thus, the possibility remains that the relationship between spindles and intelligence quotient may be an epiphenomenon of a putative relationship between good quality sleep and cognitive ability or perhaps modulated by circadian factors such as morningness-eveningness tendencies. We sought to ascertain whether spindles are directly or indirectly related to cognitive abilities using mediation analysis. Here, we show that fast (13.5-16 Hz) parietal but not slow (11-13.5 Hz) frontal spindles in both non-rapid eye movement stage 2 sleep and slow wave sleep are directly related to reasoning abilities (i.e., cognitive abilities that support "fluid intelligence," such as the capacity to identify complex patterns and relationships and the use of logic to solve novel problems) but not verbal abilities (i.e., cognitive abilities that support "crystalized intelligence"; accumulated knowledge and experience) or cognitive abilities that support STM (i.e., the capacity to briefly maintain information in an available state). The relationship between fast spindles and reasoning abilities is independent of the indicators of sleep maintenance and circadian chronotype, thus suggesting that spindles are indeed a biological marker of cognitive abilities and can serve as a window to further explore the physiological and biological substrates that give rise to human intelligence. ■

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“…In contrast, spindle frequency rhythms are seen in the isolated TRN 54,55 , but not in the isolated cortex or other thalamic nuclei 55,56 . Cortical feedback to the TRN and thalamocortical neurons, however, synchronizes spindles across cortical regions 57,58 and can initiate and terminate spindles 59 . Thus, in the intact brain, both spindles and SWs are the products of thalamocortical circuits.…”

Section: Discussionmentioning

confidence: 99%

Coordination of Slow Waves With Sleep Spindles Predicts Sleep-Dependent Memory Consolidation in Schizophrenia

Demanuele

Bartsch

Baran

et al. 2016

Sleep

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General rightsThis document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/pure/about/ebr-terms Demanuele et al., 2016 1 This study is not a clinical trial. Demanuele et al., 2016 3 Coordination of Slow Waves with Sleep Spindles Predicts Sleep-Dependent Memory Consolidation in Schizophrenia AbstractStudy Objectives: Schizophrenia patients have correlated deficits in sleep spindle density and sleep-dependent memory consolidation. In addition to spindle density, memory consolidation is thought to rely on the precise temporal coordination of spindles with slow waves (SWs). We investigated whether this coordination is intact in schizophrenia and its relation to motor procedural memory consolidation.Methods: Twenty-one chronic medicated schizophrenia patients and 17 demographicallymatched healthy controls underwent two nights of polysomnography with training on the finger tapping motor sequence task (MST) on the second night and testing the following morning. We detected SWs (0.5-4Hz) and spindles during non-rapid eye-movement (NREM) sleep. We measured SW-spindle phase-amplitude coupling and its relation with overnight improvement of MST performance.Results: Patients did not differ from controls in the timing of SW-spindle coupling. In both groups spindles peaked during the SW upstate. For patients only, the later in the SW upstate that spindles peaked and the more reliable this phase relationship, the greater the overnight MST improvement.Regression models that included both spindle density and SW-spindle coordination predicted overnight improvement significantly better than either parameter alone suggesting that both contribute to memory consolidation.Conclusions: Schizophrenia patients show intact spindle-SW temporal coordination and these timing relationships, together with spindle density, predict sleep-dependent memory consolidation.These relations were seen only in patients suggesting that their memory is more dependent on optimal spindle-SW timing, possibly due to reduced spindle density. Interventions to improve memory may need to both increase spindle density and optimize the coordination of NREM oscillations.

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Corticothalamic Feedback Controls Sleep Spindle Duration In Vivo

Cited by 177 publications

References 60 publications

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

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

Sleep Spindles and Intellectual Ability: Epiphenomenon or Directly Related?

Coordination of Slow Waves With Sleep Spindles Predicts Sleep-Dependent Memory Consolidation in Schizophrenia

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