Tumor necrosis factor enhances the sleep‐like state and electrical stimulation induces a wake‐like state in co‐cultures of neurons and glia

Jewett, Kathryn A.; Taishi, Ping; Sengupta, Parijat; Roy, Sandip; Davis, Christopher J.; Krueger, James M.

doi:10.1111/ejn.12968

Cited by 47 publications

(62 citation statements)

References 67 publications

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“…The default state of mature mixed cultures of mammalian neurons and glia is a neuronal action potential burst/pause firing pattern similar to that observed in thalamic and cortical neurons during non-rapid eye movement sleep (NREMS). 8, 9, 10, 11 To obtain such cultures, cells from murine embryos or 1–3 day old mice are used and the development of electrical activity over the course of 2–3 weeks in culture parallels developmental changes in mammalian neonatal sleep. 11 Stimulation of mature cultures with a mixed cocktail of excitatory neurotransmitters 10 or electrical pulses 11, 12 induces a wake-like state as determined by measures also used to characterize organism sleep in vivo .…”

Section: Perspectives On Sleepmentioning

confidence: 99%

“…8, 9, 10, 11 To obtain such cultures, cells from murine embryos or 1–3 day old mice are used and the development of electrical activity over the course of 2–3 weeks in culture parallels developmental changes in mammalian neonatal sleep. 11 Stimulation of mature cultures with a mixed cocktail of excitatory neurotransmitters 10 or electrical pulses 11, 12 induces a wake-like state as determined by measures also used to characterize organism sleep in vivo . Thus, upon stimulation culture gene expression profiles parallel those of an awake mouse 10 and the fraction of total action potentials occurring within a burst decreases (reduced burstiness).…”

Section: Perspectives On Sleepmentioning

confidence: 99%

“…Thus, upon stimulation culture gene expression profiles parallel those of an awake mouse 10 and the fraction of total action potentials occurring within a burst decreases (reduced burstiness). 11, 12 Further, after electrical stimulation of cultures, there is a rebound of the sleep-like state suggesting that sleep homeostasis also occurs in vitro . 11 …”

Section: Perspectives On Sleepmentioning

confidence: 99%

“…11, 12 Further, after electrical stimulation of cultures, there is a rebound of the sleep-like state suggesting that sleep homeostasis also occurs in vitro . 11 …”

Section: Perspectives On Sleepmentioning

confidence: 99%

“…13 Optogenetic stimulation of mature cultures transfected with Channelrhodopsin 2 induces release, or neuronal expression of, substances involved in sleep regulation, including adenosine triphosphate (ATP), interleukin-1 beta (IL1) and tumor necrosis factor alpha (TNF). 11 Application of TNF to the cultures induces a more intense sleep state as the burstiness, slow wave synchronization and slow wave spectral power increase; these effects are reversed during electrical stimulation. 11 If cells are taken from mice that lack the IL1 receptor neuron-specific accessory protein (called AcPb) the cells fail to respond to electrical stimulation by decreasing slow wave synchronization or delta power as do cells from wild type mice.…”

Section: Perspectives On Sleepmentioning

confidence: 99%

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Sleep function: Toward elucidating an enigma

Krueger

Frank

Wisor

et al. 2016

Sleep Medicine Reviews

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331

186

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Summary Sleep function remains controversial. Individual perspectives frame the issue of sleep function differently. We briefly illustrate how sleep measurement and the evolution, tissue organization levels, molecular mechanisms, and regulation of sleep could influence one’s view of sleep function. Then we discuss six viable theories of sleep function. Sleep serves host-defense mechanisms and conserves caloric expenditures, but these functions likely are opportunistic functions evolving later in evolution. That sleep replenishes brain energy stores and that sleep serves a glymphatic function by removing toxic byproducts of waking activity are attractive ideas, but lack extensive supporting experimental evidence. That sleep restores performance is experimentally demonstrated and has obvious evolutionary value. However, this hypothesis lacks experimentally verified mechanisms although ideas relating to this issue are presented. Finally, the ideas surrounding the broad hypothesis that sleep serves a connectivity/plasticity function are many and attractive. There is experimental evidence that connectivity changes with sleep, sleep loss, and with changing afferent input, and that those changes are linked to sleep regulatory mechanisms. In our view, this is the leading contender for the primordial function of sleep. However, much refinement of ideas and innovative experimental approaches are needed to clarify the sleep-connectivity relationship.

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Section: Perspectives On Sleepmentioning

confidence: 99%

Section: Perspectives On Sleepmentioning

confidence: 99%

Section: Perspectives On Sleepmentioning

confidence: 99%

“…11, 12 Further, after electrical stimulation of cultures, there is a rebound of the sleep-like state suggesting that sleep homeostasis also occurs in vitro . 11 …”

Section: Perspectives On Sleepmentioning

confidence: 99%

Section: Perspectives On Sleepmentioning

confidence: 99%

See 3 more Smart Citations

Sleep function: Toward elucidating an enigma

Krueger

Frank

Wisor

et al. 2016

Sleep Medicine Reviews

Self Cite

331

186

View full text Add to dashboard Cite

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Sleep- and Wake-Like States in Small Networks In Vivo and In Vitro

McKillop

Vyazovskiy

2018

Handbook of Experimental Pharmacology

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Wakefulness and sleep are highly complex and heterogeneous processes, involving multiple neurotransmitter systems and a sophisticated interplay between global and local networks of neurons and non-neuronal cells. Macroscopic approaches applied at the level of the whole organism, view sleep as a global behaviour and allow for investigation into aspects such as the effects of insufficient or disrupted sleep on cognitive function, metabolism, thermoregulation and sensory processing. While significant progress has been achieved using such large-scale approaches, the inherent complexity of sleep-wake regulation has necessitated the development of methods to tackle specific aspects of sleep in isolation. One way this may be achieved is by investigating specific cellular or molecular phenomena in the whole organism in situ, either during spontaneous or induced sleep-wake states. This approach has greatly advanced our knowledge about the electrophysiology and pharmacology of ion channels, specific receptors, intracellular pathways and the small networks implicated in control and regulation of the sleep-wake cycle. Importantly though, there are a variety of external and internal factors that influence global behavioural states which are difficult to control for using these approaches. For this reason, over the last few decades ex vivo experimental models have become increasingly popular, and have greatly advanced our understanding of many fundamental aspects of sleep, including the neuroanatomy and neurochemistry of sleep states, sleep regulation, the origin and dynamics of specific sleep oscillations, network homeostasis, as well as the functional roles of sleep. This chapter will focus on the use of small neuronal networks as experimental models and will highlight the most significant and novel insights these approaches have provided.

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